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A Fucose-Containing Sulfated Polysaccharide from Spatoglossum schröederi Potentially Targets Tumor Growth Rather Than Cytotoxicity: Distinguishing Action on Human Melanoma Cell Lines

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Abstract

Natural substances are strategic candidates for drug development in cancer research. Marine-derived molecules are of special interest due to their wide range of biological activities and sustainable large-scale production. Melanoma is a type of skin cancer that originates from genetic mutations in melanocytes. BRAF, RAS, and NF1 mutations are described as the major melanoma drivers, but approximately 20% of patients lack these mutations and are included in the triple wild-type (tripleWT) classification. Recent advances in targeted therapy directed at driver mutations along with immunotherapy have only partially improved patients’ overall survival, and consequently, melanoma remains deadly when in advanced stages. Fucose-containing sulfated polysaccharides (FCSP) are potential candidates to treat melanoma; therefore, we investigated Fucan A, a FCSP from Spatoglossum schröederi brown seaweed, in vitro in human melanoma cell lines presenting different mutations. Up to 72 h Fucan A treatment was not cytotoxic either to normal melanocytes or melanoma cell lines. Interestingly, it was able to impair the tripleWT CHL-1 cell proliferation (57%), comparable to the chemotherapeutic cytotoxic drug cisplatin results, with the advantage of not causing cytotoxicity. Fucan A increased CHL-1 doubling time, an effect attributed to cell cycle arrest. Vascular mimicry, a close related angiogenesis process, was also impaired (73%). Fucan A mode of action could be related to gene expression modulation, in special β-catenin downregulation, a molecule with protagonist roles in important signaling pathways. Taken together, results indicate that Fucan A is a potential anticancer molecule and, therefore, deserves further investigation.

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Availability of Data and Material

The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Abbreviations

WT:

Wild-type

FCSP:

Fucose-containing sulfated polysaccharide

NIH:

National Institutes of Health

UPH2O:

Ultra-pure water

FBS:

Fetal bovine serum

DMEM:

Dulbecco’s Modified Eagle’s Medium

CV:

Crystal violet

NR:

Neutral red

PFA:

Paraformaldehyde

BSA:

Bovine serum albumin

PPI:

Protein-protein interactions

FA:

Fucan A

VM:

Vasculogenic mimicry

DEGs:

Differentially expressed genes

GO:

Gene ontology

SEM:

Standard error of measurement

ECM:

Extracellular matrix

References

  • Abe S, Hiramatsu K, Ichikawa O et al (2013) Safety evaluation of excessive ingestion of mozuku fucoidan in human. J Food Sci 78:T648–T651

    CAS  PubMed  Google Scholar 

  • Alexandrov LB, Nik-Zainal S, Wedge DC et al (2013) Signatures of mutational processes in human cancer. Nature 500:415–421

    CAS  PubMed  PubMed Central  Google Scholar 

  • Almeida-Lima J, Costa LS, Silva NB et al (2010) Evaluating the possible genotoxic, mutagenic and tumor cell proliferation-inhibition effects of a non-anticoagulant, but antithrombotic algal heterofucan. J Appl Toxicol 30:708–715

    CAS  PubMed  Google Scholar 

  • Almeida-Lima J, Dantas-Santos N, Gomes DL et al (2011) Evaluation of acute and subchronic toxicity of a non-anticoagulant, but antithrombotic algal heterofucan from the Spatoglossum schröederi in Wistar rats. Rev Bras Farmacogn 21:674–679

    CAS  Google Scholar 

  • Arias-Mejias SM, Warda KY, Quattrocchi E et al (2020) The role of integrins in melanoma: a review. Int J Dermatol 59:525–534

    CAS  PubMed  PubMed Central  Google Scholar 

  • Atashrazm F, Lowenthal RM, Woods GM et al (2015) Fucoidan and cancer: a multifunctional molecule with anti-tumor potential. Mar Drugs 13:2327–2346

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barroso EMA, Costa LS, Medeiros VP et al (2008) A non-anticoagulant heterofucan has antithrombotic activity in vivo. Planta Med 74:712–718

    CAS  PubMed  Google Scholar 

  • Bellan DL, Bini IH, Santi FC et al (2023) Fucoidan from Spatoglossum schröederi promotes B16–F10 malignancy features modulation and antimelanoma in vivo activities. Algal Res 72:103134

    Google Scholar 

  • Bienz M (2005) Beta-catenin: a pivot between cell adhesion and Wnt signalling. Curr Biol 15:R64–R67

    CAS  PubMed  Google Scholar 

  • Blaszczak W, Lach MS, Barczak W, Suchorska WM (2018) Fucoidan exerts anticancer effects against head and neck squamous cell carcinoma in vitro. Molecules 23. https://doi.org/10.3390/molecules23123302

  • Boo H-J, Hong J-Y, Kim S-C et al (2013) The anticancer effect of fucoidan in PC-3 prostate cancer cells. Mar Drugs 11:2982–2999

    PubMed  PubMed Central  Google Scholar 

  • Brás MM, Radmacher M, Sousa SR, Granja PL (2020) Melanoma in the eyes of mechanobiology. Front Cell Dev Biol 8:54

    PubMed  PubMed Central  Google Scholar 

  • Brenner E, Schörg BF, Ahmetlić F et al (2020) Cancer immune control needs senescence induction by interferon-dependent cell cycle regulator pathways in tumours. Nat Commun 11:1335

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • National Comprehensive Cancer Network® (NCCN®) (2018) NCCN Guidelines for Patients®: Melanoma 2018

  • Cancer Genome Atlas Network (2015) Genomic classification of cutaneous melanoma. Cell 161:1681–1696

    Google Scholar 

  • Che J-P, Li W, Yan Y et al (2013) Expression and clinical significance of the nin one binding protein and p38 MAPK in prostate carcinoma. Int J Clin Exp Pathol 6:2300–2311

    PubMed  PubMed Central  Google Scholar 

  • Chen M-C, Hsu W-L, Hwang P-A, Chou T-C (2015) Low molecular weight fucoidan inhibits tumor angiogenesis through downregulation of HIF-1/VEGF signaling under hypoxia. Mar Drugs 13:4436–4451

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Cong Q, Du Z et al (2016) Sulfated fucoidan FP08S2 inhibits lung cancer cell growth in vivo by disrupting angiogenesis via targeting VEGFR2/VEGF and blocking VEGFR2/Erk/VEGF signaling. Cancer Lett 382:44–52

    CAS  PubMed  Google Scholar 

  • Cho T-M, Kim W-J, Moon S-K (2014) AKT signaling is involved in fucoidan-induced inhibition of growth and migration of human bladder cancer cells. Food Chem Toxicol 64:344–352

    CAS  PubMed  Google Scholar 

  • Choo G-S, Lee H-N, Shin S-A et al (2016) Anticancer effect of fucoidan on DU-145 prostate cancer cells through inhibition of PI3K/Akt and MAPK pathway expression. Mar Drugs 14. https://doi.org/10.3390/md14070126

  • Citkowska A, Szekalska M, Winnicka K (2019) Possibilities of fucoidan utilization in the development of pharmaceutical dosage forms. Mar Drugs 17. https://doi.org/10.3390/md17080458

  • ClinicalTrials.gov. https://clinicaltrials.gov/ct2/home. Accessed 27 May 2022a

  • Cong Q, Chen H, Liao W et al (2016) Structural characterization and effect on anti-angiogenic activity of a fucoidan from Sargassum fusiforme. Carbohydr Polym 136:899–907

    CAS  PubMed  Google Scholar 

  • Conway JR, Dietlein F, Taylor-Weiner A et al (2020) Integrated molecular drivers coordinate biological and clinical states in melanoma. Nat Genet 52:1373–1383

    CAS  PubMed  PubMed Central  Google Scholar 

  • Corban M, Ambrose M, Pagnon J et al (2019) Pathway analysis of fucoidan activity using a yeast gene deletion library screen. Mar Drugs 17. https://doi.org/10.3390/md17010054

  • Darzynkiewicz Z, Juan G, Li X et al (1997) Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry 27:1–20

    CAS  PubMed  Google Scholar 

  • Corrêa FDM, Guerra RL, Fernandes RRA et al (2019) Target therapy versus dacarbazine in first-line treatment of advanced non-surgical and metastatic melanoma: budget impact analysis from the perspective of the Brazilian National Health System, 2018–2020. Epidemiol Serv Saude 28:e2018325

  • DeLeon TT, Almquist DR, Kipp BR et al (2020) Assessment of clinical outcomes with immune checkpoint inhibitor therapy in melanoma patients with CDKN2A and TP53 pathogenic mutations. PLoS ONE 15:e0230306

    CAS  PubMed  PubMed Central  Google Scholar 

  • Delgado-Bellido D, Serrano-Saenz S, Fernández-Cortés M, Oliver FJ (2017) Vasculogenic mimicry signaling revisited: focus on non-vascular VE-cadherin. Mol Cancer 16:65

    PubMed  PubMed Central  Google Scholar 

  • Domingues B, Lopes JM, Soares P, Pópulo H (2018) Melanoma Treatment in Review Immunotargets Ther 7:35–49

    CAS  PubMed  Google Scholar 

  • Dörschmann P, Kopplin G, Roider J, Klettner A (2019) Effects of sulfated fucans from regarding vegf secretion, cell viability, and oxidative stress and correlation with molecular weight. Mar Drugs 17. https://doi.org/10.3390/md17100548

  • Dyshlovoy SA, Honecker F (2019) Marine compounds and cancer: the first two decades of XXI century. Mar Drugs 18. https://doi.org/10.3390/md18010020

  • Etman SM, Elnaggar YSR, Abdallah OY (2020) Fucoidan, a natural biopolymer in cancer combating: from edible algae to nanocarrier tailoring. Int J Biol Macromol 147:799–808

    CAS  PubMed  Google Scholar 

  • Fernández-Cortés M, Delgado-Bellido D, Javier Oliver F (2019) Vasculogenic mimicry: become an endothelial cell “but not so much.” Front Oncol 9

  • Galluzzi L, Spranger S, Fuchs E, López-Soto A (2019) WNT signaling in cancer immunosurveillance. Trends Cell Biol 29:44–65

    CAS  PubMed  Google Scholar 

  • Garman B, Anastopoulos IN, Krepler C et al (2017) Genetic and genomic characterization of 462 melanoma patient-derived xenografts, tumor biopsies, and cell lines. Cell Rep 21:1936–1952

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gene - NCBI - COL11A1 collagen type XI alpha 1 chain [Homo sapiens (human)]. http://www.ncbi.nlm.nih.gov/gene/1301. Accessed 31 May 2021d

  • Gene - NCBI - COL6A2 collagen type VI alpha 2 chain [Homo sapiens (human)]. http://www.ncbi.nlm.nih.gov/gene/1292. Accessed 31 May 2021b

  • Gene - NCBI - COL8A1 collagen type VIII alpha 1 chain [Homo sapiens (human)]. http://www.ncbi.nlm.nih.gov/gene/1295. Accessed 31 May 2021c

  • Gene - NCBI - ITGA1 integrin subunit alpha 1 [Homo sapiens (human)]. http://www.ncbi.nlm.nih.gov/gene/3672. Accessed 31 May 2021e

  • Gene - NCBI - ITGA4 integrin subunit alpha 4 [Homo sapiens (human)]. http://www.ncbi.nlm.nih.gov/gene/3676. Accessed 31 May 2021h

  • Gene - NCBI - ITGB3 integrin subunit beta 3 [Homo sapiens (human)]. http://www.ncbi.nlm.nih.gov/gene/3690. Accessed 31 May 2021g

  • Gene - NCBI - ITGB4 integrin subunit beta 4 [Homo sapiens (human)]. http://www.ncbi.nlm.nih.gov/gene/3691. Accessed 31 May 2021f

  • Gershenwald JE, Scolyer RA, Hess KR et al (2017) Melanoma staging: evidence-based changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin 67:472–492

  • Gillies RJ, Didier N, Denton M (1986) Determination of cell number in monolayer cultures. Anal Biochem 159:109–113

    CAS  PubMed  Google Scholar 

  • Gueven N, Spring KJ, Holmes S et al (2020) Micro RNA expression after ingestion of fucoidan; a clinical study. Mar Drugs 18. https://doi.org/10.3390/md18030143

  • Haggag YA, Abd Elrahman AA, Ulber R, Zayed A (2023) Fucoidan in pharmaceutical formulations: a comprehensive review for smart drug delivery systems. Mar Drugs 21. https://doi.org/10.3390/md21020112

  • Hainaut P, Pfeifer GP (2016) Somatic TP53 mutations in the era of genome sequencing. Cold Spring Harb Perspect Med 6. https://doi.org/10.1101/cshperspect.a026179

  • Han Z, Ni J, Smits P et al (2001) Extracellular matrix protein 1 (ECM1) has angiogenic properties and is expressed by breast tumor cells. FASEB J 15:988–994

    CAS  PubMed  Google Scholar 

  • Han Y-S, Lee JH, Lee SH (2015) Antitumor effects of fucoidan on human colon cancer cells via activation of Akt signaling. Biomol Ther 23:225–232

    CAS  Google Scholar 

  • Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674

    CAS  PubMed  Google Scholar 

  • Haneji K, Matsuda T, Tomita M et al (2005) Fucoidan extracted from Cladosiphon okamuranus Tokida induces apoptosis of human T-cell leukemia virus type 1-infected T-cell lines and primary adult T-cell leukemia cells. Nutr Cancer 52:189–201

    CAS  PubMed  Google Scholar 

  • Hansen NUB, Willumsen N, Sand JMB et al (2016) Type VIII collagen is elevated in diseases associated with angiogenesis and vascular remodeling. Clin Biochem 49:903–908

    CAS  PubMed  Google Scholar 

  • Hasselström L, Thomas J-B, Nordström J et al (2020) Socioeconomic prospects of a seaweed bioeconomy in Sweden. Sci Rep 10:1610

    PubMed  PubMed Central  ADS  Google Scholar 

  • Hendrix MJ, Seftor EA, Meltzer PS et al (2001) Expression and functional significance of VE-cadherin in aggressive human melanoma cells: role in vasculogenic mimicry. Proc Natl Acad Sci U S A 98:8018–8023

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Hendrix MJC, Seftor EA, Seftor REB et al (2016) Tumor cell vascular mimicry: novel targeting opportunity in melanoma. Pharmacol Ther 159:83–92

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hilke FJ, Sinnberg T, Gschwind A et al (2020) Distinct mutation patterns reveal melanoma subtypes and influence immunotherapy response in advanced melanoma patients. Cancers 12. https://doi.org/10.3390/cancers12092359

  • Hsu H-Y, Hwang P-A (2019) Clinical applications of fucoidan in translational medicine for adjuvant cancer therapy. Clin Transl Med 8:15

    PubMed  PubMed Central  Google Scholar 

  • INCA - Estudos clínicos com inscrições abertas no INCA. https://www.gov.br/inca/pt-br/assuntos/pesquisa/ensaios-clinicos/estudos-clinicos-com-inscricoes-abertas-no-inca/protocolos-de-pele. Accessed 6 July 2023

  • Ishii T, Konishi T, Yamasaki T et al (2010) NMR characterization of acidic xylo-oligosaccharides containing two methylglucuronic acid residues from Japanese cedar and Hinoki cypress. Carbohydr Polym 81:964–968

    CAS  Google Scholar 

  • Isnansetyo A, Laili Lutfia FN, Nursid M et al (2016) Cytotoxicity of fucoidan from three tropical brown algae against breast and colon cancer cell lines. PJ 9:14–20

  • January GG, Naidoo RK, Kirby-McCullough B, Bauer R (2019) Assessing methodologies for fucoidan extraction from South African brown algae. Algal Res 40:101517

    Google Scholar 

  • Kageshita T, Hamby CV, Ishihara T et al (2001) Loss of beta-catenin expression associated with disease progression in malignant melanoma. Br J Dermatol 145:210–216

    CAS  PubMed  Google Scholar 

  • Kawahara R, Niwa Y, Simizu S (2018) Integrin β1 is an essential factor in vasculogenic mimicry of human cancer cells. Cancer Sci 109:2490–2496

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khalifa SAM, Elias N, Farag MA et al (2019) Marine natural products: a source of novel anticancer drugs. Mar Drugs 17. https://doi.org/10.3390/md17090491

  • Kim I-H, Nam T-J (2018) Fucoidan downregulates insulin-like growth factor-I receptor levels in HT-29 human colon cancer cells. Oncol Rep 39:1516–1522

    CAS  PubMed  Google Scholar 

  • Kirschmann DA, Seftor EA, Hardy KM et al (2012) Molecular pathways: vasculogenic mimicry in tumor cells: diagnostic and therapeutic implications. Clin Cancer Res 18:2726–2732

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kovacs D, Migliano E, Muscardin L et al (2016) The role of Wnt/β-catenin signaling pathway in melanoma epithelial-to-mesenchymal-like switching: evidences from patients-derived cell lines. Oncotarget 7:43295–43314

    PubMed  PubMed Central  Google Scholar 

  • Lal G, Contreras PG, Kulak M et al (2013) Human melanoma cells over-express extracellular matrix 1 (ECM1) which is regulated by TFAP2C. PLoS ONE 8:e73953

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Lamandé SR, Bateman JF (2018) Collagen VI disorders: insights on form and function in the extracellular matrix and beyond. Matrix Biol 71–72:348–367

    PubMed  Google Scholar 

  • Lauden L, Siewiera J, Boukouaci W et al (2014) TGF-β-induced (TGFBI) protein in melanoma: a signature of high metastatic potential. J Invest Dermatol 134:1675–1685

    CAS  PubMed  Google Scholar 

  • Laurens LML, Lane M, Nelson RS (2020) Sustainable seaweed biotechnology solutions for carbon capture, composition, and deconstruction. Trends Biotechnol 38:1232–1244

    CAS  PubMed  Google Scholar 

  • Leite EL, Medeiros MGL, Rocha HAO et al (1998) Structure and pharmacological activities of a sulfated xylofucoglucuronan from the alga Spatoglossum schröederi. Plant Sci 132:215–228

    CAS  Google Scholar 

  • Leonard MK, Novak M, Snyder D et al (2019) The metastasis suppressor NME1 inhibits melanoma cell motility via direct transcriptional induction of the integrin beta-3 gene. Exp Cell Res 374:85–93

    CAS  PubMed  Google Scholar 

  • Liu X, Wang X, Du W et al (2014) Suppressor of fused (Sufu) represses Gli1 transcription and nuclear accumulation, inhibits glioma cell proliferation, invasion and vasculogenic mimicry, improving glioma chemo-sensitivity and prognosis. Oncotarget 5:11681–11694

    PubMed  PubMed Central  Google Scholar 

  • Liu F, Luo G, Xiao Q et al (2016) Fucoidan inhibits angiogenesis induced by multiple myeloma cells. Oncol Rep 36:1963–1972

    CAS  PubMed  Google Scholar 

  • Liu M, Tolg C, Turley E (2019) Dissecting the dual nature of hyaluronan in the tumor microenvironment. Front Immunol 10:947

    CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) Method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Makino E, Gutmann V, Kosnopfel C et al (2018) Melanoma cells resistant towards MAPK inhibitors exhibit reduced TAp73 expression mediating enhanced sensitivity to platinum-based drugs. Cell Death Dis 9:930

    PubMed  PubMed Central  Google Scholar 

  • Maniotis AJ, Folberg R, Hess A et al (1999) Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 155:739–752

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mansour MB, Balti R, Yacoubi L et al (2019) Primary structure and anticoagulant activity of fucoidan from the sea cucumber Holothuria polii. Int J Biol Macromol 121:1145–1153

    PubMed  Google Scholar 

  • Mason R, Au L, Ingles Garces A, Larkin J (2019) Current and emerging systemic therapies for cutaneous metastatic melanoma. Expert Opin Pharmacother 20:1135–1152

    PubMed  Google Scholar 

  • Mazepa E, Biscaia SM, Bellan DL et al (2022) Structural characteristics of native and chemically sulfated polysaccharides from seaweed and their antimelanoma effects. Carbohydr Polym 289:119436

  • Menezes MM, Nobre LTDB, Rossi GR et al (2018) A low-molecular-weight galactofucan from the seaweed, Spatoglossum schröederi, binds fibronectin and inhibits capillary-like tube formation in vitro. Int J Biol Macromol 111:1067–1075

    CAS  PubMed  Google Scholar 

  • Menshova RV, Anastyuk SD, Ermakova SP et al (2015) Structure and anticancer activity in vitro of sulfated galactofucan from brown alga Alaria angusta. Carbohydr Polym 132:118–125

    CAS  PubMed  Google Scholar 

  • Min E-Y, Kim I-H, Lee J et al (2014) The effects of fucodian on senescence are controlled by the p16INK4a-pRb and p14Arf-p53 pathways in hepatocellular carcinoma and hepatic cell lines. Int J Oncol 45:47–56

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nemlich Y, Besser MJ, Schachter J, Markel G (2020) ADAR1 regulates melanoma cell invasiveness by controlling beta3-integrin via microRNA-30 family members. Am J Cancer Res 10:2677–2686

    CAS  PubMed  PubMed Central  Google Scholar 

  • Newman DJ, Cragg GM (2016) Natural products as sources of new drugs from 1981 to 2014. J Nat Prod 79:629–661

    CAS  PubMed  Google Scholar 

  • Nummela P, Lammi J, Soikkeli J et al (2012) Transforming growth factor beta-induced (TGFBI) is an anti-adhesive protein regulating the invasive growth of melanoma cells. Am J Pathol 180:1663–1674

    CAS  PubMed  Google Scholar 

  • Palkina N, Komina A, Aksenenko M et al (2018) miR-204-5p and miR-3065-5p exert antitumor effects on melanoma cells. Oncol Lett 15:8269–8280

    PubMed  PubMed Central  Google Scholar 

  • Papadas A, Arauz G, Cicala A et al (2020) Versican and versican-matrikines in cancer progression, inflammation, and immunity. J Histochem Cytochem 68:871–885

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park HS, Hwang HJ, Kim G-Y et al (2013) Induction of apoptosis by fucoidan in human leukemia U937 cells through activation of p38 MAPK and modulation of Bcl-2 family. Mar Drugs 11:2347–2364

    PubMed  PubMed Central  Google Scholar 

  • Park HY, Kim G-Y, Moon S-K et al (2014) Fucoidan inhibits the proliferation of human urinary bladder cancer T24 cells by blocking cell cycle progression and inducing apoptosis. Molecules 19:5981–5998

    PubMed  PubMed Central  Google Scholar 

  • Park HY, Choi I-W, Kim G-Y et al (2015) Fucoidan induces G1 arrest of the cell cycle in EJ human bladder cancer cells through down-regulation of pRB phosphorylation. Rev Bras Farmacogn 25:246–251

    CAS  Google Scholar 

  • Pearce A, Haas M, Viney R et al (2017) Incidence and severity of self-reported chemotherapy side effects in routine care: a prospective cohort study. PLoS One 12:e0184360

    PubMed  PubMed Central  Google Scholar 

  • Poukka M, Bykachev A, Siiskonen H et al (2016) Decreased expression of hyaluronan synthase 1 and 2 associates with poor prognosis in cutaneous melanoma. BMC Cancer 16:313

    PubMed  PubMed Central  Google Scholar 

  • Pradeep CR, Sunila ES, Kuttan G (2005) Expression of vascular endothelial growth factor (VEGF) and VEGF receptors in tumor angiogenesis and malignancies. Integr Cancer Ther 4:315–321

    CAS  PubMed  Google Scholar 

  • Rani V (2017) Influence of species, geographic location, seasonal variation and extraction method on the fucoidan yield of the brown seaweeds of gulf of Mannar, India. Indian J Pharm Sci 79

  • Repetto G, del Peso A, Zurita JL (2008) Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc 3:1125–1131

    CAS  PubMed  Google Scholar 

  • Reuben A, Spencer CN, Prieto PA et al (2017) Genomic and immune heterogeneity are associated with differential responses to therapy in melanoma. NPJ Genom Med 2. https://doi.org/10.1038/s41525-017-0013-8

  • Reyes ME, Riquelme I, Salvo T et al (2020) Brown seaweed fucoidan in cancer: implications in metastasis and drug resistance. Mar Drugs 18. https://doi.org/10.3390/md18050232

  • Rocha Amorim MO, Lopes Gomes D, Dantas LA et al (2016) Fucan-coated silver nanoparticles synthesized by a green method induce human renal adenocarcinoma cell death. Int J Biol Macromol 93:57–65

    CAS  PubMed  Google Scholar 

  • Rubanyi GM (1999) Angiogenesis in health and disease: basic mechanisms and clinical applications. CRC Press, Boca Raton, FL

    Google Scholar 

  • Saeed AFUH, Su J, Ouyang S (2021) Marine-derived drugs: recent advances in cancer therapy and immune signaling. Biomed Pharmacother 134:111091

    CAS  PubMed  Google Scholar 

  • Seftor REB, Hess AR, Seftor EA et al (2012) Tumor cell vasculogenic mimicry: from controversy to therapeutic promise. Am J Pathol 181:1115–1125

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shain AH, Yeh I, Kovalyshyn I et al (2015) The genetic evolution of melanoma from precursor lesions. N Engl J Med 373:1926–1936

    PubMed  Google Scholar 

  • Siiskonen H, Poukka M, Tyynelä-Korhonen K et al (2013) Inverse expression of hyaluronidase 2 and hyaluronan synthases 1–3 is associated with reduced hyaluronan content in malignant cutaneous melanoma. BMC Cancer 13:181

    CAS  PubMed  Google Scholar 

  • Simas FF, Gorin PAJ, Guerrini M et al (2004) Structure of a heteroxylan of gum exudate of the palm Scheelea phalerata (uricuri). Phytochemistry 65:2347–2355

    CAS  PubMed  Google Scholar 

  • Sinnberg T, Menzel M, Ewerth D et al (2011) β-Catenin signaling increases during melanoma progression and promotes tumor cell survival and chemoresistance. PLoS One 6:e23429

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Song Y, Mu L, Han X et al (2013) MicroRNA-9 inhibits vasculogenic mimicry of glioma cell lines by suppressing Stathmin expression. J Neurooncol 115:381–390

    CAS  PubMed  Google Scholar 

  • Sun B, Zhang S, Zhao X et al (2004) Vasculogenic mimicry is associated with poor survival in patients with mesothelial sarcomas and alveolar rhabdomyosarcomas. Int J Oncol. https://doi.org/10.3892/ijo.25.6.1609

    Article  PubMed  Google Scholar 

  • Sun T, Zhao N, Zhao X-L et al (2010) Expression and functional significance of Twist1 in hepatocellular carcinoma: its role in vasculogenic mimicry. Hepatology 51:545–556

    CAS  PubMed  Google Scholar 

  • Takabe P, Bart G, Ropponen A et al (2015) Hyaluronan synthase 3 (HAS3) overexpression downregulates MV3 melanoma cell proliferation, migration and adhesion. Exp Cell Res 337:1–15

    CAS  PubMed  Google Scholar 

  • Tan LY, Mintoff C, Johan MZ et al (2016) Desmoglein 2 promotes vasculogenic mimicry in melanoma and is associated with poor clinical outcome. Oncotarget 7:46492–46508

    PubMed  PubMed Central  Google Scholar 

  • Tan LY, Martini C, Fridlender ZG et al (2017) Control of immune cell entry through the tumour vasculature: a missing link in optimising melanoma immunotherapy? Clin Transl Immunology 6:e134

    PubMed  PubMed Central  Google Scholar 

  • Teng H, Yang Y, Wei H et al (2015) Fucoidan suppresses hypoxia-induced lymphangiogenesis and lymphatic metastasis in mouse hepatocarcinoma. Mar Drugs 13:3514–3530

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tomić K, Tica Sedlar I, Berić Jozić G et al (2018) Complete response of metastatic melanoma to second line chemotherapy with paclitaxel and carboplatin - case report. Acta Med Acad 47:82–87

    PubMed  Google Scholar 

  • Toss MS, Miligy IM, Gorringe KL et al (2019) Collagen (XI) alpha-1 chain is an independent prognostic factor in breast ductal carcinoma in situ. Mod Pathol 32:1460–1472

    CAS  PubMed  Google Scholar 

  • Tsai H-L, Tai C-J, Huang C-W et al (2017) Efficacy of low-molecular-weight fucoidan as a supplemental therapy in metastatic colorectal cancer patients: a double-blind randomized controlled trial. Mar Drugs 15. https://doi.org/10.3390/md15040122

  • Usoltseva RV, Anastyuk SD, Ishina IA et al (2018) Structural characteristics and anticancer activity in vitro of fucoidan from brown alga Padina boryana. Carbohydr Polym 184:260–268

    CAS  PubMed  Google Scholar 

  • Vanni I, Tanda ET, Dalmasso B et al (2020) Non-BRAF mutant melanoma: molecular features and therapeutical implications. Front Mol Biosci 7:172

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vartanian A, Stepanova E, Grigorieva I et al (2011) VEGFR1 and PKCα signaling control melanoma vasculogenic mimicry in a VEGFR2 kinase-independent manner. Melanoma Res 21:91–98

    CAS  PubMed  Google Scholar 

  • Vartanian A, Karshieva S, Dombrovsky V, Belyavsky A (2016) Melanoma educates mesenchymal stromal cells towards vasculogenic mimicry. Oncol Lett 11:4264–4268

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vizkeleti L, Kiss T, Koroknai V et al (2017) Altered integrin expression patterns shown by microarray in human cutaneous melanoma. Melanoma Res 27:180–188

    CAS  PubMed  Google Scholar 

  • Vlad-Fiegen A, Langerak A, Eberth S, Müller O (2012) The Wnt pathway destabilizes adherens junctions and promotes cell migration via β-catenin and its target gene cyclin D1. FEBS Open Bio 2:26–31

    PubMed  PubMed Central  Google Scholar 

  • Wang P, Liu Z, Liu X et al (2014) Anti-metastasis effect of fucoidan from Undaria pinnatifida sporophylls in mouse hepatocarcinoma Hca-F cells. PLoS One 9:e106071

    PubMed  PubMed Central  ADS  Google Scholar 

  • Wang Z, Li Z, Wang Y et al (2015) Versican silencing improves the antitumor efficacy of endostatin by alleviating its induced inflammatory and immunosuppressive changes in the tumor microenvironment. Oncol Rep 33:2981–2991

    CAS  PubMed  Google Scholar 

  • Wang M, Jiang S, Zhou L et al (2019a) Potential mechanisms of action of curcumin for cancer prevention: focus on cellular signaling pathways and miRNAs. Int J Biol Sci 15:1200–1214

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Xing M, Cao Q et al (2019b) Biological activities of fucoidan and the factors mediating its therapeutic effects: a review of recent studies. Mar Drugs 17. https://doi.org/10.3390/md17030183

  • Wilson MA, Schuchter LM (2016) Chemotherapy for melanoma. Cancer Treat Res 167:209–229

    PubMed  Google Scholar 

  • Wu L, Sun J, Su X et al (2016a) A review about the development of fucoidan in antitumor activity: Progress and challenges. Carbohydr Polym 154:96–111

    CAS  PubMed  Google Scholar 

  • Wu S-Y, Wu ATH, Yuan KS-P, Liu SH (2016b) Brown seaweed fucoidan inhibits cancer progression by dual regulation of mir-29c/ADAM12 and miR-17-5p/PTEN axes in human breast cancer cells. J Cancer 7:2408–2419

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wynne MJ (1986) A checklist of benthic marine algae of the tropical and subtropical western Atlantic. Can J Bot 64:2239–2281

    Google Scholar 

  • Xu S, Xu H, Wang W et al (2019) The role of collagen in cancer: from bench to bedside. J Transl Med 17:309

    PubMed  PubMed Central  Google Scholar 

  • Xue M, Ge Y, Zhang J et al (2012) Anticancer properties and mechanisms of fucoidan on mouse breast cancer in vitro and in vivo. PLoS One 7:e43483

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Young RJ, Waldeck K, Martin C et al (2014) Loss of CDKN2A expression is a frequent event in primary invasive melanoma and correlates with sensitivity to the CDK4/6 inhibitor PD0332991 in melanoma cell lines. Pigment Cell Melanoma Res 27:590–600

    CAS  PubMed  Google Scholar 

  • Zhan T, Rindtorff N, Boutros M (2017) Wnt signaling in cancer. Oncogene 36:1461–1473

    CAS  PubMed  Google Scholar 

  • Zhang Z, Imani S, Shasaltaneh MD et al (2019) The role of vascular mimicry as a biomarker in malignant melanoma: a systematic review and meta-analysis. BMC Cancer 19:1134

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou L, Yang K, Wickett RR et al (2016) Targeted deactivation of cancer-associated fibroblasts by β-catenin ablation suppresses melanoma growth. Tumour Biol 37:14235–14248

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to acknowledge the facility “Centro de Tecnologias Avançadas em Fluorescência – CTAF/UFPR” for fluorescence and confocal microscopy support; Dr. Lucelia Donatti for experimental support on spectrophotometer use; Dr. Silvio S Veiga for support on PCR experiments; Dr. Karin B Prado for flow cytometry support; Dr. Gustavo R Rossi, Dr. Jenifer P Gonçalves, and Dr. Helena B Nader for technical support; and Dr. Roger Chammas for kindly providing the cell lines and for technical support.

Funding

The following grants partially supported this work: Brazilian funding agencies CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) financial support (Grant numbers: CAPES- 001-CIMAR 1985/2014; PROCAD 2965/2014; PROAP/PPGBCM-UFPR) and student’s fellowships. UFPR/PRPG - research financial support (grant approved on 04/2018 UFPR/PRPPG “Apoio a atividades de pesquisa” call).

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Authors and Affiliations

  1. Cell Biology Department, Universidade Federal Do Paraná (UFPR), Curitiba, Paraná, Brazil

    Maíra Barbosa e Reis, Açucena Imparato Maximo, Jessica Maria Magno, Daniel de Lima Bellan, João Luiz Aldinucci Buzzo, Fernanda Fogagnoli Simas, Edvaldo da Silva Trindade & Carolina Camargo de Oliveira

  2. Biochemistry Department, Centro de Biociências, Universidade Federal do Rio Grande do Norte (UFRN), Natal, Rio Grande do Norte, Brazil

    Hugo Alexandre Oliveira Rocha

Authors
  1. Maíra Barbosa e Reis
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  2. Açucena Imparato Maximo
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  3. Jessica Maria Magno
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  4. Daniel de Lima Bellan
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  8. Edvaldo da Silva Trindade
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  9. Carolina Camargo de Oliveira
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Contributions

MBR: conceptualization, methodology, validation, formal analysis, investigation, writing—original draft, and writing—review and editing. AIM: methodology, validation, formal analysis, investigation, and review and editing. DLB: validation and writing—review and editing. JMM: methodology, validation, investigation, and review and editing. JLAB: methodology, validation, and review and editing. FFS: validation, formal analysis, and writing—review and editing. HAOR: conceptualization, methodology, project administration, funding acquisition, and review and editing. EST: conceptualization, resources, writing—review and editing, supervision, funding acquisition, review, and editing. CCO: conceptualization, validation, resources, supervision, project administration, funding acquisition, and writing—review and editing.

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Correspondence to Carolina Camargo de Oliveira.

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Reis, M.B.e., Maximo, A.I., Magno, J.M. et al. A Fucose-Containing Sulfated Polysaccharide from Spatoglossum schröederi Potentially Targets Tumor Growth Rather Than Cytotoxicity: Distinguishing Action on Human Melanoma Cell Lines. Mar Biotechnol 26, 181–198 (2024). https://doi.org/10.1007/s10126-024-10287-y

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