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Perspective| Volume 21, ISSUE 2, e126-e134, June 2022

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Targeting Hyaluronic Acid and Peritoneal Dissemination in Colorectal Cancer

  • Faris Soliman
    Correspondence
    Address for correspondence: Faris Soliman, MBBCh MRCS Cardiff China Medical Research Unit, Henry Wellcome Building, University Hospital Wales, Cardiff, CF14 4XW, UK
    Affiliations
    Cardiff China Medical Research Collaborative, Division of Cancer and Genetics, School of Medicine, Cardiff University

    Cardiff and Vale University Health Board
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  • Lin Ye
    Affiliations
    Cardiff China Medical Research Collaborative, Division of Cancer and Genetics, School of Medicine, Cardiff University
    Search for articles by this author
  • Wenguo Jiang
    Affiliations
    Cardiff China Medical Research Collaborative, Division of Cancer and Genetics, School of Medicine, Cardiff University
    Search for articles by this author
  • Rachel Hargest
    Affiliations
    Cardiff China Medical Research Collaborative, Division of Cancer and Genetics, School of Medicine, Cardiff University

    Cardiff and Vale University Health Board
    Search for articles by this author
Published:November 28, 2021DOI:https://doi.org/10.1016/j.clcc.2021.11.008

      Abstract

      Peritoneal metastasis (PM) from colorectal cancer (CRC) carries a significant mortality rate for patients and treatment is challenging. The development of PM is a multistep process involving detachment, adhesion, invasion and colonization of the peritoneal cavity. Cytoreductive surgery and HIPEC (hyperthermic intraperitoneal chemotherapy) for PM from CRC has some benefit but overall survival is poor and recurrence rates are high. Treatments to prevent the development of peritoneal metastasis could have the potential to improve CRC survival and disease-free outcomes.
      The ability of cancer cells to invade the peritoneum and become established as metastatic tumors is influenced by a multifactorial process. Hyaluronic acid (HA) has been shown to coat the mesothelial cells of the peritoneum and has been demonstrated to be utilized in various malignancies as part of the metastatic process in peritoneal dissemination. CD44, RHAMM (CD168) and ICAM-1 have all been shown to be binding partners for HA. Targeting HA-mediated binding may prevent adhesion to distant sites within the peritoneum through suppression of interaction of these molecules. Here we review the current literature and discuss key molecules involved with PM dissemination, with the potential to target these mechanisms in the delivery of future treatments.

      Keywords

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      References

        • Torre L.A.
        • Bray F.
        • Siegel R.L.
        • et al.
        Global cancer statistics.
        CA Cancer J Clin. 2012; 65 (2015): 87-108
        • Suthananthan A.E.
        • Bhandari M.
        • Platell C.
        Influence of primary site on metastatic distribution and survival in stage IV colorectal cancer.
        ANZ J Surg. 2017; 88: 445-449https://doi.org/10.1111/ans.13969
        • Sugarbaker P.H.
        Peritoneal surface oncology: review of a personal experience with colorectal and appendiceal malignancy.
        Tech Coloproctol. 2005; 9: 95-103
        • Sugarbaker P.H.
        Colorectal carcinomatosis: a new oncologic frontier.
        Curr Opin Oncol. 2005; 17: 397-399
        • Hermanek P.
        • Wittekind C.
        The pathologist and the residual tumor (R) classification.
        Pathol Res Pract. 1994; 190: 115-123
        • Sato H.
        • Kotake K.
        • Sugihara K.
        • et al.
        Clinicopathological factors associated with recurrence and prognosis after R0 resection for stage IV colorectal cancer with peritoneal metastasis.
        Dig Surg. 2016; 33: 382-391
        • Jayne D.G.
        • Fook S.
        • Loi C.
        • Seow-Choen F.
        • et al.
        Peritoneal carcinomatosis from colorectal cancer.
        Br J Surg. 2002; 89: 1545-1550
        • Sadler T.W.a.L.
        Langman's Medical Embryology.
        (J) Wolters Kluwer Health/Lippincott Williams & Wilkins Philadelphia, 2012
        • van Baal J.O.
        • Van de Vijver K.K.
        • Nieuwland R.
        • et al.
        The histophysiology and pathophysiology of the peritoneum.
        Tissue Cell. 2017; 49: 95-105
        • Evanko S.P.
        • Tammi M.I.
        • Tammi R.H.
        • Wight T.N.
        • et al.
        Hyaluronan-dependent pericellular matrix.
        Adv Drug Deliv Rev. 2007; 59: 1351-1365
        • Knudson C.B.
        • Munaim S.I.
        • Toole B.P.
        Ectodermal stimulation of the production of hyaluronan-dependent pericellular matrix by embryonic limb mesodermal cells.
        Dev Dyn. 1995; 204: 186-191
        • Tammi M.I.
        • Day A.J.
        • Turley E.A.
        Hyaluronan and homeostasis: a balancing act.
        J Biol Chem. 2002; 277: 4581-4584
        • Weigel P.H.
        • DeAngelis P.L.
        Hyaluronan synthases: a decade-plus of novel glycosyltransferases.
        J Biol Chem. 2007; 282: 36777-36781
        • Weigel P.H.
        • Hascall V.C.
        • Tammi M.
        Hyaluronan synthases.
        J Biol Chem. 1997; 272: 13997-14000
        • Laurent T.C.
        • Laurent U.B.
        • Fraser J.R.
        The structure and function of hyaluronan: an overview.
        Immunol Cell Biol. 1996; 74: A1-A7
        • Laurent T.C.
        • Fraser J.R.
        Hyaluronan.
        FASEB J. 1992; 6: 2397-2404
        • Knudson W.
        • Chow G.
        • Knudson C.B.
        CD44-mediated uptake and degradation of hyaluronan.
        Matrix Biol. 2002; 21: 15-23
        • Laurent U.B.G.
        • Reed R.K.
        Turnover of Hyaluronan in the Tissues.
        Adv Drug Del Rev. 1991; 7: 237-256
        • Mutsaers S.E.
        Mesothelial cells: their structure, function and role in serosal repair.
        Respirology. 2002; 7: 171-191
        • Mironov V.A.
        • Gusev S.A.
        • Baradi A.F.
        Mesothelial stomata overlying omental milky spots: scanning electron microscopic study.
        Cell Tissue Res. 1979; 201: 327-330
        • Mutsaers S.E.
        • Prele C.M.
        • Pengelly S.
        • Herrick S.E.
        • et al.
        Mesothelial cells and peritoneal homeostasis.
        Fertil Steril. 2016; 106: 1018-1024
        • Mutsaers S.E.
        • Birnie K.
        • Lansley S.
        • et al.
        Mesothelial cells in tissue repair and fibrosis.
        Front Pharmacol. 2015; 6: 113
        • Raftery A.T.
        Regeneration of parietal and visceral peritoneum: an electron microscopical study.
        J Anat. 1973; 115: 375-392
      1. Nolph, K.D., Peritoneal Anatomy and Transport Physiology, in Replacement of Renal Function by Dialysis, P.F.M. Drukker W., Maher J.F., Editor. 1983, Springer, Dordrecht.

        • Foley-Comer A.J.
        • Herrick S.E.
        • Al-Mishlab T.
        • et al.
        Evidence for incorporation of free-floating mesothelial cells as a mechanism of serosal healing.
        J Cell Sci. 2002; 115: 1383-1389
        • Blackburn S.C.
        • Stanton M.P.
        Anatomy and physiology of the peritoneum.
        Semin Pediatr Surg. 2014; 23: 326-330
        • Albanese A.M.
        • Albanese E.F.
        • Mino J.H.
        • et al.
        Peritoneal surface area: measurements of 40 structures covered by peritoneum: correlation between total peritoneal surface area and the surface calculated by formulas.
        Surg Radiol Anat. 2009; 31: 369-377
        • Rubin J.
        • Clawson M.
        • Planch A.
        • Jones Q.
        • et al.
        Measurements of peritoneal surface area in man and rat.
        Am J Med Sci. 1988; 295: 453-458
        • Meyers M.A.
        Distribution of intra-abdominal malignant seeding: dependency on dynamics of flow of ascitic fluid.
        Am J Roentgenol Radium Ther Nucl Med. 1973; 119: 198-206
        • Canbay E Y.Y.
        Molecular Mechanism of Peritoneal Metastases.
        Peritoneal Surface Malignancies. Springer, Cham2015
        • Yonemura Y.C.E.
        • Liu Y
        • Elnemr A
        • Endo Y.
        • Miura M.
        • Ishibashi H.
        • et al.
        Trans-lymphatic metastasis in peritoneal dissemination.
        J Gastrointest Digest Syst. 2013; S12
        • Alkhamesi N.A.
        • Ziprin P.
        • Pfistermuller K.
        • Peck D.H.
        • Darzi A.W.
        • et al.
        ICAM-1 mediated peritoneal carcinomatosis, a target for therapeutic intervention.
        Clin Exp Metastasis. 2005; 22: 449-459
        • Jonjic N.
        • Peri G.
        • Bernasconi S.
        • et al.
        Expression of adhesion molecules and chemotactic cytokines in cultured human mesothelial cells.
        J Exp Med. 1992; 176: 1165-1174
        • Liu Y.
        • Bunston C.
        • Hodson N.
        • et al.
        Psoriasin promotes invasion, aggregation and survival of pancreatic cancer cells; association with disease progression.
        Int J Oncol. 2017; 50: 1491-1500
        • van Grevenstein W.M.
        • Hofland L.J.
        • van Rossen M.E.
        • et al.
        Inflammatory cytokines stimulate the adhesion of colon carcinoma cells to mesothelial monolayers.
        Dig Dis Sci. 2007; 52: 2775-2783
        • Klein C.L.
        • Bittinger F.
        • Skarke C.C.
        • et al.
        Effects of cytokines on the expression of cell adhesion molecules by cultured human omental mesothelial cells.
        Pathobiology. 1995; 63: 204-212
        • Heath R.M.
        • Jayne D.G.
        • O’Leary R.
        • Morrison E.E.
        • Guillou P.J.
        • et al.
        Tumour-induced apoptosis in human mesothelial cells: a mechanism of peritoneal invasion by Fas Ligand/Fas interaction.
        Br J Cancer. 2004; 90: 1437-1442
        • Yonemura Y.
        • Endou Y.
        • Nojima M.
        • et al.
        A possible role of cytokines in the formation of peritoneal dissemination.
        Int J Oncol. 1997; 11: 349-358
        • Davies D.E.
        • Farmer S.
        • White J.
        • et al.
        Contribution of host-derived growth factors to in vivo growth of a transplantable murine mammary carcinoma.
        Br J Cancer. 1994; 70: 263-269
        • Saeki T.
        • Salomon D.S.
        • Johnson G.R.
        • et al.
        Association of epidermal growth factor-related peptides and type I receptor tyrosine kinase receptors with prognosis of human colorectal carcinomas.
        Jpn J Clin Oncol. 1995; 25: 240-249
        • Hanahan D.
        • Weinberg R.A.
        Hallmarks of cancer: the next generation.
        Cell. 2011; 144: 646-674
        • Lemoine L.
        • Sugarbaker P.
        • Van der Speeten K.
        Pathophysiology of colorectal peritoneal carcinomatosis: role of the peritoneum.
        World J Gastroenterol. 2016; 22: 7692-7707
        • McCourt P.A.
        • Ek B.
        • Forsberg N.
        • Gustafson S.
        • et al.
        Intercellular adhesion molecule-1 is a cell surface receptor for hyaluronan.
        J Biol Chem. 1994; 269: 30081-30084
        • Entwistle J.
        • Zhang S.
        • Yang B.
        • et al.
        Characterization of the murine gene encoding the hyaluronan receptor RHAMM.
        Gene. 1995; 163: 233-238
        • Aruffo A.
        • Stamenkovic I.
        • Melnick M.
        • Underhill C.B.
        • Seed B.
        • et al.
        CD44 is the principal cell surface receptor for hyaluronate.
        Cell. 1990; 61: 1303-1313
        • Ahrens T.
        • Assmann V.
        • Fieber C.
        • et al.
        CD44 is the principal mediator of hyaluronic-acid-induced melanoma cell proliferation.
        J Invest Dermatol. 2001; 116: 93-101
        • Kim Y.
        • Kumar S.
        CD44-mediated adhesion to hyaluronic acid contributes to mechanosensing and invasive motility.
        Mol Cancer Res. 2014; 12: 1416-1429
        • Lokeshwar V.B.
        • Mirza S.
        • Jordan A.
        Targeting hyaluronic acid family for cancer chemoprevention and therapy.
        Adv Cancer Res. 2014; 123: 35-65
        • Jordan A.R.
        • Racine R.R.
        • Hennig M.J.
        • Lokeshwar V.B.
        • et al.
        The role of CD44 in disease pathophysiology and targeted treatment.
        Front Immunol. 2015; 6: 182
        • Sneath R.J.
        • Mangham D.C.
        The normal structure and function of CD44 and its role in neoplasia.
        Mol Pathol. 1998; 51: 191-200
        • Lesley J.
        • Hyman R.
        CD44 structure and function.
        Front Biosci. 1998; 3: d616-d630
        • Siegelman M.H.
        • DeGrendele H.C.
        • Estess P.
        Activation and interaction of CD44 and hyaluronan in immunological systems.
        J Leukoc Biol. 1999; 66: 315-321
        • Johnson P.
        • Ruffell B.
        CD44 and its role in inflammation and inflammatory diseases.
        Inflamm Allergy Drug Targets. 2009; 8: 208-220
        • Gao A.C.
        • Lou W.
        • Dong J.T.
        • Isaacs J.T.
        • et al.
        CD44 is a metastasis suppressor gene for prostatic cancer located on human chromosome 11p13.
        Cancer Res. 1997; 57: 846-849
        • Cooper D.L.
        • Dougherty G.
        • Harn H.J.
        • et al.
        The complex CD44 transcriptional unit; alternative splicing of three internal exons generates the epithelial form of CD44.
        Biochem Biophys Res Commun. 1992; 182: 569-578
        • Gunthert U.
        • Hofmann M.
        • Rudy W.
        • et al.
        A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells.
        Cell. 1991; 65: 13-24
        • Schutze A.
        • Vogeley C.
        • Gorges T.
        • et al.
        RHAMM splice variants confer radiosensitivity in human breast cancer cell lines.
        Oncotarget. 2016; 7: 21428-21440
        • Hall C.L.
        • Turley E.A.
        Hyaluronan: RHAMM mediated cell locomotion and signaling in tumorigenesis.
        J Neurooncol. 1995; 26: 221-229
        • Zhang S.
        • Chang M.C.
        • Zylka D.
        • et al.
        The hyaluronan receptor RHAMM regulates extracellular-regulated kinase.
        J Biol Chem. 1998; 273: 11342-11348
        • Wang C.
        • Thor A.D.
        • Moore D.H.
        • et al.
        The overexpression of RHAMM, a hyaluronan-binding protein that regulates ras signaling, correlates with overexpression of mitogen-activated protein kinase and is a significant parameter in breast cancer progression.
        Clin Cancer Res. 1998; 4: 567-576
        • Hall C.L.
        • Wang C.
        • Lange L.A.
        • Turley E.A.
        • et al.
        Hyaluronan and the hyaluronan receptor RHAMM promote focal adhesion turnover and transient tyrosine kinase activity.
        J Cell Biol. 1994; 126: 575-588
        • Alkhamesi N.A.
        • Roberts G.
        • Ziprin P.
        • Peck D.H.
        • et al.
        Induction of proteases in peritoneal carcinomatosis, the Role of ICAM-1/CD43 interaction.
        Biomark Insights. 2007; 2: 377-384
        • Mikula-Pietrasik J.
        • Uruski P.
        • Kucinska M.
        • Tykarski A.
        • Ksiazek K.
        • et al.
        The protective activity of mesothelial cells against peritoneal growth of gastrointestinal tumors: The role of soluble ICAM-1.
        Int J Biochem Cell Biol. 2017; 86: 26-31
        • Maeda K.
        • Kang S.M.
        • Sawada T.
        • et al.
        Expression of intercellular adhesion molecule-1 and prognosis in colorectal cancer.
        Oncol Rep. 2002; 9: 511-514
        • Peach R.J.
        • Hollenbaugh D.
        • Stamenkovic I.
        • Aruffo A.
        • et al.
        Identification of hyaluronic acid binding sites in the extracellular domain of CD44.
        J Cell Biol. 1993; 122: 257-264
        • Liu D.
        • Sy M.S.
        A cysteine residue located in the transmembrane domain of CD44 is important in binding of CD44 to hyaluronic acid.
        J Exp Med. 1996; 183: 1987-1994
        • Kellett-Clarke H.
        • Stegmann M.
        • Barclay A.N.
        • Metcalfe C.
        • et al.
        CD44 binding to hyaluronic acid is redox regulated by a labile disulfide bond in the hyaluronic acid binding site.
        PLoS ONE [Electronic Resource]. 2015; 10e0138137
        • Elliott V.A.
        • Rychahou P.
        • Zaytseva Y.Y.
        • Evers B.M.
        • et al.
        Activation of c-Met and upregulation of CD44 expression are associated with the metastatic phenotype in the colorectal cancer liver metastasis model.
        PLoS ONE [Electronic Resource]. 2014; 9: e97432
        • Wangpu X.
        • Yang X.
        • Zhao J.
        • et al.
        The metastasis suppressor, NDRG1, inhibits “stemness” of colorectal cancer via down-regulation of nuclear beta-catenin and CD44.
        Oncotarget. 2015; 6: 33893-33911
        • Zeilstra J.
        • Joosten S.P.
        • Vermeulen L.
        • et al.
        CD44 expression in intestinal epithelium and colorectal cancer is independent of p53 status.
        PLoS One. 2013; 8: e72849
        • Yamane N.
        • Tsujitani S.
        • Makino M.
        • Maeta M.
        • Kaibara N.
        • et al.
        Soluble CD44 variant 6 as a prognostic indicator in patients with colorectal cancer.
        Oncology. 1999; 56: 232-238
        • Yamaguchi A.
        • Goi T.
        • Taguchi S.
        • et al.
        Clinical significance of serum levels of CD44 variant exons 8-10 protein in colorectal cancer.
        J Gastroenterol. 1998; 33: 349-353
        • Wielenga V.J.
        • van der Voort R.
        • Mulder J.W
        • et al.
        CD44 splice variants as prognostic markers in colorectal cancer.
        Scand J Gastroenterol. 1998; 33: 82-87
        • Weg-Remers S.
        • Schuder G.
        • Zeitz M.
        • Stallmach A.
        • et al.
        CD44 expression in colorectal cancer.
        Ann N Y Acad Sci. 1998; 859: 304-306
        • Katoh S.
        • Goi T.
        • Naruse T.
        • et al.
        Cancer stem cell marker in circulating tumor cells: expression of CD44 variant exon 9 is strongly correlated to treatment refractoriness, recurrence and prognosis of human colorectal cancer.
        Anticancer Res. 2015; 35: 239-244
        • Fujisaki T.
        • Tanaka Y.
        • Fujii K.
        • et al.
        CD44 stimulation induces integrin-mediated adhesion of colon cancer cell lines to endothelial cells by up-regulation of integrins and c-Met and activation of integrins.
        Cancer Res. 1999; 59: 4427-4434
        • Hirota-Takahata Y.
        • Harada H.
        • Tanaka I.
        • et al.
        F-19848 A, a novel inhibitor of hyaluronic acid binding to cellular receptor CD44.
        J Antibiot. 2007; 60: 633-639
        • Hirota-Takahata Y.
        • Harada H.
        • Tanaka I.
        • et al.
        F-16438s, novel binding inhibitors of CD44 and hyaluronic acid. II. Producing organism, fermentation, isolation, physico-chemical properties and structural elucidation.
        J Antibiot. 2006; 59: 777-784
        • Turley E.A.
        Purification of a hyaluronate-binding protein fraction that modifies cell social behavior.
        Biochem Biophys Res Commun. 1982; 108: 1016-1024
        • Turley E.A.
        • Torrance J.
        Localization of hyaluronate and hyaluronate-binding protein on motile and non-motile fibroblasts.
        Exp Cell Res. 1985; 161: 17-28
        • Turley E.A.
        • Moore D.
        • Hayden L.J.
        Characterization of hyaluronate binding proteins isolated from 3T3 and murine sarcoma virus transformed 3T3 cells.
        Biochemistry. 1987; 26: 2997-3005
        • Turley E.A.
        The role of a cell-associated hyaluronan-binding protein in fibroblast behaviour.
        Ciba Found Symp. 1989; 143 (discussion 133-7, 281-5): 121-133
        • Turley E.A.
        Hyaluronan and cell locomotion.
        Cancer Metastasis Rev. 1992; 11: 21-30
        • Yang B.
        • Yang B.L.
        • Savani R.C.
        • Turley E.A.
        • et al.
        Identification of a common hyaluronan binding motif in the hyaluronan binding proteins RHAMM, CD44 and link protein.
        EMBO J. 1994; 13: 286-296
        • Wang K.
        • Zhang T.
        Prognostic significance of CD168 overexpression in colorectal cancer.
        Oncol Lett. 2016; 12: 2555-2559
        • Mele V.
        • Sokol L.
        • Kolzer V.H.
        • et al.
        The hyaluronan-mediated motility receptor RHAMM promotes growth, invasiveness and dissemination of colorectal cancer.
        Oncotarget. 2017; 8: 70617-70629
        • Koelzer V.H.
        • Huber B.
        • Mele V.
        • et al.
        Expression of the hyaluronan-mediated motility receptor RHAMM in tumor budding cells identifies aggressive colorectal cancers.
        Hum Pathol. 2015; 46: 1573-1581
        • de Cuba E.M.
        • Kwakman R.
        • van Egmond M.
        • et al.
        Understanding molecular mechanisms in peritoneal dissemination of colorectal cancer: future possibilities for personalised treatment by use of biomarkers.
        Virchows Arch. 2012; 461: 231-243
        • Gibbs P.
        • Clingan P.R.
        • Ganju V.
        • et al.
        Hyaluronan-Irinotecan improves progression-free survival in 5-fluorouracil refractory patients with metastatic colorectal cancer: a randomized phase II trial.
        Cancer Chemother Pharmacol. 2011; 67: 153-163
        • Clinicaltrials.gov
        Trial of FOLF(HA)Iri With Cetuximab in mCRC (Chime).
        ClinicalTrials.gov Identifier: NCT02216487, 2014 ([cited 2019 10th January 2019]; Available at)
      2. Clinicaltrials.gov. Trial of FOLF(HA)Iri Versus FOLFIRI in mCRC (FOLF(HA)iri). ClinicalTrials.gov Identifier: NCT01290783. 2015 [cited 2019 10th January 2019]; Available at: https://clinicaltrials.gov/ct2/show/NCT01290783?id=NCT01290783+OR+NCT02216487&rank=2&load=cart.

        • Shariati M.
        • Lollo G.
        • Matha K.
        • et al.
        Synergy between Intraperitoneal Aerosolization (PIPAC) and cancer nanomedicine: cisplatin-loaded polyarginine-hyaluronic acid nanocarriers efficiently eradicate peritoneal metastasis of advanced human ovarian cancer.
        ACS Appl Mater Interfaces. 2020; 12: 29024-29036
        • Strobel T.
        • Swanson L.
        • Cannistra S.A.
        In vivo inhibition of CD44 limits intra-abdominal spread of a human ovarian cancer xenograft in nude mice: a novel role for CD44 in the process of peritoneal implantation.
        Cancer Res. 1997; 57: 1228-1232
        • Menke-van der Houven van Oordt C.W.
        • Gomez-Roca C.
        • van Herpen C.
        • et al.
        First-in-human phase I clinical trial of RG7356, an anti-CD44 humanized antibody, in patients with advanced, CD44-expressing solid tumors.
        Oncotarget. 2016; 7: 80046-80058
        • de Lima Vazquez V.
        • Stuart O.A.
        • Mohamed F.
        • Sugarbaker P.H.
        • et al.
        Extent of parietal peritonectomy does not change intraperitoneal chemotherapy pharmacokinetics.
        Cancer Chemother Pharmacol. 2003; 52: 108-112