CC BY 4.0 · AIMS Genet 2018; 05(01): 075-090
DOI: 10.3934/genet.2018.1.75
Review

Esophageal cancer research today and tomorrow: Lessons from algae and other perspectives

Vladlena Tiasto
1   Centre for Genomic and Regenerative Medicine, School of Biomedicine, FEFU, 8 Sukhanova str, Vladivostok, Primorsky region, 690950, Russian Federation
,
Valeriia Mikhailova
1   Centre for Genomic and Regenerative Medicine, School of Biomedicine, FEFU, 8 Sukhanova str, Vladivostok, Primorsky region, 690950, Russian Federation
,
Valeriia Gulaia
1   Centre for Genomic and Regenerative Medicine, School of Biomedicine, FEFU, 8 Sukhanova str, Vladivostok, Primorsky region, 690950, Russian Federation
,
Valeriia Vikhareva
2   Laboratory of Pharmacology and Bioassays, School of Biomedicine, FEFU, 8 Sukhanova str, Vladivostok, Primorsky region, 690950, Russian Federation
,
Boris Zorin
3   Microalgal Biotechnology Laboratory, The French Associates Institute for Agriculture and Biotechnology for Drylands, The J. Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, Midreshet Ben-Gurion 8499000, Israel
,
Alexandra Kalitnik
2   Laboratory of Pharmacology and Bioassays, School of Biomedicine, FEFU, 8 Sukhanova str, Vladivostok, Primorsky region, 690950, Russian Federation
,
Alexander Kagansky
1   Centre for Genomic and Regenerative Medicine, School of Biomedicine, FEFU, 8 Sukhanova str, Vladivostok, Primorsky region, 690950, Russian Federation
› Author Affiliations

Abstract

Esophageal cancer is an increasing concern due to poor prognosis, aggressive disease modalities, and a lack of efficient therapeutics. The two types of esophageal cancer: esophageal squamous cell carcinoma (ESCC) and esophageal adenocarcinoma (EAC) are responsible for an estimated 450,000 annual deaths, with over 457,000 new patients diagnosed in 2015, making it the eighth most prevalent and the 10th most fatal cancer worldwide. As esophageal cancer prevalence continues to increase, and so does the pressing need for the development of new and effective strategies for the early diagnostics, prevention, and treatment of this cancer, as well for building the innovative research tools to understand the affected molecular mechanisms.

This short review summarizes the current statistics and recent research of the problems and solutions related to the esophageal cancer, and offer a brief overview of its epidemiology, molecular alterations, and existing biomedical tools. We will discuss currently available research tools and discuss selected approaches we deem relevant to find new model systems and therapies for the future with the special focus on novel opportunities presented by the unique molecules found in algae, namely carbohydrates and lipids. Their remarkable chemical variability is connected to their striking structural and functional properties, which combined with the relative novelty of these compounds to cancer biology, warrants interest of the wide biomedical community to these molecules, especially in the esophageal cancer theory and practice.



Publication History

Received: 02 December 2017

Accepted: 01 March 2018

Article published online:
10 May 2021

© 2018. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Song Q, Jiang D, Wang H. et al. Chromosomal and genomic variations in esophageal squamous cell carcinoma: A review of technologies, applications, and prospections. J Cancer 2017; 8: 2492
  • 2 Hou X, Wen J, Ren Z. et al. Non-coding RNAs: New biomarkers and therapeutic targets for esophageal cancer. Oncotarget 2017; 8: 43571-43578
  • 3 Esophagus Cancer statictics in USA. Esophagus Cancer.org. [Online] June 14, 2017. Available from: www.cancer.org/cancer/esophaguscancer/detailedguide/esophagus-cancer-key-statistics
  • 4 Testa U, Castelli G, Pelosi E. Esophageal cancer: Genomic and molecular characterization, stem cell compartment and clonal evolution. Medicinis 2017;4
  • 5 Esophageal cancer statistics in UK. Cancer Research UK. [Online] Nov 22, 2017. Available from: www.cancerresearchuk.org/health-professional/cancer-statistics/statistics-by-cancer-type/oesophageal-cancer#heading-One
  • 6 Zhang Y. Epidemiology of esophageal cancer. World J Gastroenterol 2013; 19: 5598-5606
  • 7 Taylor PR, Abnet CC, Dawsey SM. Squamous dysplasia  the precursor lesion for esophageal squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 2013; 22: 540-552
  • 8 Siewert JR, Ott K. Are squamous and adenocarcinomas of the esophagus the same disease?. Semin Radiat Oncol 2007; 17: 38-44
  • 9 Zhao R, Young CB, Mee-Hyun L. et al. Implications of genetic and epigenetic alterations of CDKN2A (p16INK4a) in cancer. Ebiomedicine 2016; 8: 30-39
  • 10 Singhi AD, Foxwell TJ, Nason K. et al. Smad4 loss in esophageal adenocarcinoma is associated with an increased propensity for disease recurrence and poor survival. Am J Surg Pathol 2015; 39: 487-495
  • 11 Streppel MM, Lata S, DelaBastide M. et al. Next-generation sequencing of endoscopic biopsies identifies ARID1A as a tumor-suppressor gene in Barrett's esophagus. Oncogene 2014; 33: 347-357
  • 12 Dulak AM, Stojanov P, Peng S. et al. Exome and whole-genome sequencing of esophageal adenocarcinoma identifies recurrent driver events and mutational complexity. Nat Genet 2013; 45: 478-486
  • 13 Gao YB, Chen ZL, Li JG. et al. Genetic landscape of esophageal squamous cell carcinoma. Nat Genet 2014; 46: 1097-1102
  • 14 Sasaki Y, Tamura M, Koyama R. et al. Genomic characterization of esophageal squamous cell carcinoma: Insights from next-generation sequencing. World J Gastroenterol 2016; 22: 2284-2293
  • 15 Nazila N, Katrien VR, Mohammad V. et al. Expression, Tissue Distribution and Function of miR-21 in Esophageal Squamous Cell Carcinoma. PLoS One 2013; 8: e73009
  • 16 Rubenstein JH, Shaheen NJ. Epidemiology, diagnosis, and management of esophageal adenocarcinoma. Gastroenterology 2015; 149: 302-317
  • 17 Watanabe M. Risk factors and molecular mechanisms of esophageal cancer: Differences between the histologic subtypes. J Cancer Metastasis Treat 2015; 1: 1-7
  • 18 Halland M, Katzka D, Iyer PG. Recent developments in pathogenesis, diagnosis and therapy of Barrett's esophagus. World J Gastroenterol 2015; 21: 6479-6490
  • 19 Palethorpe HM, Drew PA, Smith E. Androgen Signaling in Esophageal Adenocarcinoma Cell Lines In Vitro . Dig Dis Sci 2017; 62: 3402-3414
  • 20 Wang RH. From reflux esophagitis to Barrett's esophagus and esophageal adenocarcinoma. World J Gastroenterol 2015; 21: 5210-5219
  • 21 Pietsch EC, Humbey O, Murphy ME. Polymorphisms in the p53 pathway. Oncogene 2006; 25: 1602-1611
  • 22 Bond G, Hu W, Bond EE. et al. A single nucleotide polymorphism in the MDM2 promoter. Cell 2004; 119: 591-602
  • 23 Akbari M, Malekzadeh R, Lepage P. et al. Mutations in Fanconi anemia genes and the risk of esophageal cancer. Hum Genet 2011; 129: 573-582
  • 24 Dandara C, Li DP, Walther G. et al. Gene-environment interaction: The role of SULT1A1 and CYP3A5 polymorphisms as risk modifiers for squamous cell. Carcinogenesis 2006; 27: 791-797
  • 25 O'Neill JR, Pak HS, Pairocastineira E. et al. Quantitative Shotgun Proteomics Unveils Candidate Novel Esophageal Adenocarcinoma (EAC)-Specific Proteins. Mol Cell Proteomics Mcp 2017; 16: 1138-1150
  • 26 Ke X, Yan R, Sun Z. et al. Esophageal Adenocarcinoma—Derived Extracellular Vesicle MicroRNAs Induce a Neoplastic Phenotype in Gastric Organoids. Neoplasia 2017; 19: 941-949
  • 27 Lee Y, Urbanska AM, Hayakawa Y. et al. Gastrin stimulates a cholecystokinin-2-receptor-expressing cardia progenitor cell and promotes progression of Barrett's-like esophagus. Oncotarget 2016; 8: 203-214
  • 28 D'Journo XB, Thomas PA. Current management of esophageal cancer. J Thorac Dis 2014; 6: S253-S264
  • 29 Sohda M, Kuwano H. Current Status and Future Prospects for Esophageal Cancer Treatment. Ann Thorac Cardiovasc Surg 2016; 23: 1-11
  • 30 Akutsu Y, Matsubara H. Chemoradiotherapy and surgery for T4 esophageal cancer in Japan. Surg Today 2015; 45: 1360-1365
  • 31 Sithranga BN, Kathiresan K. Anticancer drugs from marine flora: An overview. J Oncol 2011; 2010: 214186
  • 32 Tebbutt NC, Price TJ, Ferraro DA. et al. Panitumumab added to docetaxel, cisplatin and fluoropyrimidine in oesophagogastric cancer: ATTAX3 phase II trial. Br J Cancer 2016; 114: 505-509
  • 33 Niu J, Gelbspan D, Weitz D. et al. HER2-positive, trastuzumab-resistant metastatic esophageal cancer presenting with brain metastasis after durable response to dual HER2 blockade: A case report. J Gastrointest Oncol 2014; 5: E103-E110
  • 34 Idelevich E, Kashtan H, Klein Y. et al. Prospective phase II study of neoadjuvant therapy with cisplatin, 5-FU, and bevacizumab for locally advanced resectable esophageal cancer. Onkologie 2012; 35: 427-431
  • 35 Davidson M, Starling N. Trastuzumab in the management of gastroesophageal cancer: Patient selection and perspectives. OncoTargets Ther 2016; 9: 7235-7245
  • 36 Ilson DH, Kelsen D, Shah M. et al. A phase 2 trial of erlotinib in patients with previously treated squamous cell and adenocarcinoma of the esophagusr. Cancer 2011; 117: 1409-1414
  • 37 Rodriguez CP, Adelstein DJ, Rice TW. et al. A phase II study of perioperative concurrent chemotherapy, gefitinib, and hyperfractionated radiation followed by maintenance gefitinib in locoregionally advanced esophagus and gastroesophageal junction cancer. J Thorac Oncol 2010; 5: 229-235
  • 38 Altiok S, Mezzadra H, Jagannath S. et al. A novel pharmacodynamic approach to assess and predict tumor response to the epidermal growth factor receptor inhibitor gefitinib in patients with esophageal cancer. Int J Oncol 2010; 36: 19
  • 39 Martinucci I, Bortoli ND, Russo S. et al. Barrett's esophagus in 2016: From pathophysiology to treatment. World J Gastrointest Pharmacol Ther 2016; 7: 190-206
  • 40 Kwiatek MA, Roman S, Fareeduddin A. et al. An alginate-antacid formulation (Gaviscon Double Action Liquid) can eliminate the postprandial “acid pocket” in symptomatic GERD patients. Aliment Pharmacol Ther 2011; 34: 59-66
  • 41 Yuan H, Song J, Li X. et al. Immunomodulation and antitumor activity of k-carrageenan oligosaccharides. Cancer Lett 2006; 243: 228-234
  • 42 Monnerat C, Faivre S, Temam S. et al. End points for new agents in induction chemotherapy for locally advanced head and neck cancers. Ann Oncol 2002; 13: 995-1006
  • 43 Neergheen-Bhujun V, Awan AT, Baran Y. et al. Biodiversity, drug discovery, and the future of global health: Introducing the biodiversity to biomedicine consortium, a call to action. J Global Health 2017; 7: 20304
  • 44 Jimeno J, Faircloth G, Sousa-Faro JF. et al. New Marine Derived Anticancer Therapeutics—A Journey from the Sea to Clinical Trials. Mar Drugs 2004; 2: 14-29
  • 45 Kijjoa A, Sawangwong P. Drugs and Cosmetics from the Sea. Mar Drugs 2004; 2: 328-336
  • 46 Kuo YH, Liang TW, Liu KC. et al. Isolation and identification of a novel antioxidant with antitumour activity from Serratia ureilytica using squid pen as fermentation substrate. Mar Biotechnol 2011; 13: 451-461
  • 47 Kwon HJ, Bae SY, Kim KH. et al. Induction of apoptosis in HeLa cells by ethanolic extract of Corallina pilulifera. Food Chem 2007; 104: 196-201
  • 48 Lins KOAL, Bezerra DP, Alves APNN. et al. Antitumor properties of a sulfated polysaccharide from the red seaweed Champia feldmannii (Diaz-Pifferer). J Appl Toxicol Jat 2009; 29: 20-26
  • 49 Thoppil RJ, Bishayee A. Terpenoids as potential chemopreventive and therapeutic agents in liver cancer. World J Hepatol 2011; 3: 228-249
  • 50 Zandi K, Ahmadzadeh S, Tajbakhsh S. et al. Anticancer activity of Sargassum oligocystum water extract against human cancer cell lines. Eur Rev Med Pharmacol Sci 2010; 14: 669-673
  • 51 Usoltseva RV, Anastyuk SD, Shevchenko NM. et al. Polysaccharides from brown algae Sargassum duplicatum: The structure and anticancer activity in vitro . Carbohydr Polym 2017; 175: 547-556
  • 52 Alves C, Pinteus S, Horta A. et al. High cytotoxicity and anti-proliferative activity of algae extracts on an in vitro model of human hepatocellular carcinoma. Springerplus 2016; 5: 1339
  • 53 Gamal-Eldeen AM, Ahmed EF, Abo-Zeid MA. In vitro cancer chemopreventive properties of polysaccharide extract from the brown alga, Sargassum latifolium. Food Chem Toxicol 2009; 47: 1378-1384
  • 54 Foley SA, Mulloy B, Tuohy MG. et al. An unfractionated fucoidan from Ascophyllum nodosum: Extraction, characterization, and apoptotic effects in vitro . J Nat Prod 2011; 74: 1851-1861
  • 55 Jiang Z, Okimura T, Yokose T. Effects of sulfated fucan, ascophyllan, from the brown Alga Ascophyllum nodosum on various cell lines: A comparative study on ascophyllan and fucoidan. J Biosci Bioeng 2010; 110: 113-117
  • 56 Zhang Z, Kiichiro T, Hiroshi E. et al. Fucoidan extract induces apoptosis in MCF-7 cells via a mechanism involving the ROS-dependent JNK activation and mitochondria-mediated pathways. PLoS One 2011; 6: e27441
  • 57 Jiao G, Yu G, Zhang J. et al. Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 2011; 9: 196-223
  • 58 Cumashi A, Ushakova NA, Preobrazhenskaya ME. et al. A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 2007; 17: 541-552
  • 59 Hyun J, Kim S, Kang J. et al. Apoptosis inducing activity of fucoidan in HCT-15 colon carcinoma cells. Biol Pharm Bull 2009; 32: 1760-1764
  • 60 Park HS, Kim GY, Nam TJ. et al. Antiproliferative activity of fucoidan was associated with the induction of apoptosis and autophagy in AGS human gastric cancer cells. J Food Sci 2011; 76: T77-T83
  • 61 Luo M, Shao B, Nie W. et al. Antitumor and Adjuvant Activity of Λ-carrageenan by Stimulating Immune Response in Cancer Immunotherapy. Sci Rep 2015; 5: 11062
  • 62 Jazzara M, Ghannam A, Soukkarieh C. et al. Anti-Proliferative Activity of Λ-Carrageenan Through the Induction of Apoptosis in Human Breast Cancer Cells. Iran J Cancer Prev 2016; 9: e3836
  • 63 Yuan Y, Song J, Li X. et al. Enhanced immunostimulatory and antitumor activity of different derivatives of kappa-carrageenan oligosaccharides from Kappaphycus striatum. J Appl Phycol 2011; 23: 59-65
  • 64 Fedorov SN, Ermakova SP, Zvyagintseva TN. et al. Anticancer and Cancer Preventive Properties of Marine Polysaccharides: Some Results and Prospects. Mar Drugs 2013; 11: 4876-4901
  • 65 Yermak IM, Barabanova AO, Aminin DL. et al. Effects of structural peculiarities of carrageenans on their immunomodulatory and anticoagulant activities. Carbohydr Polym 2012; 87: 713-720
  • 66 Kalitnik AA, Anastyuk SD, Sokolova EV. et al. Oligosaccharides of k/Β-carrageenan from the red alga Tichocarpus crinitus and their ability to induce interleukin 10. J Appl Phycol 2016; 28: 545-553
  • 67 Thomson AW, Fowler EF. Carrageenan: A review of its effects on the immune system. Agents Actions 1981; 11: 265-273
  • 68 Morais-Zani KD, Nunes FPB, Silva JBD. et al. The anti-inflammatory action of Bothrops jararaca snake antithrombin on acute inflammation induced by carrageenan in mice. Inflammation Res 2013; 62: 733-742
  • 69 Tsuji R, Hoshino K, Noro Y. et al. Suppression of allergic reaction by Λ-carrageenan: Toll-like receptor 4/MyD88-dependent and -independent modulation of immunity. Clin Exp Allergy 2003; 33: 249-258
  • 70 Garcia AM, Chaly ES. Preliminary spherical agglomerates of water-soluble drug using natural polymer and cross-linking technique. J Controlled Release 1996; 40: 179-186
  • 71 Schmidt AG, Wartewig S, Picker KM. Potential of carrageenans to protect drugs from polymorphic transformation. Eur J Pharm Biopharm 2003; 56: 101-110
  • 72 Thommes M, Kleinebudde P. Use of kappa-carrageenan as alternative pelletisation aid to microcrystalline cellulose in extrusion/spheronisation. I. Influence of type and fraction of filler. Eur J Pharm Biopharm 2006; 63: 59-67
  • 73 Hugerth AM. Micropolarity and microviscosity of amitriptyline and dextran sulfate/carrageenan-amitriptyline systems: The nature of polyelectrolyte-drug complexes. J Pharm Sci 2001; 90: 1665-1677
  • 74 Patil RT, Speaker TJ. Water-based microsphere delivery system for proteins. J Pharm Sci 2000; 89: 9-15
  • 75 Yermak IM, Khotimchenko YS. Chemical properties, biological activities and applications of carrageenan from red algae. Recent Adv Mar Biotechnol 2003; 9: 207-255
  • 76 Volod'ko AV, Davydova VN, Chusovitin E. et al. Soluble chitosan carrageenan polyelectrolyte complexes and their gastroprotective activity. Carbohydr Polym 2014; 101: 1087
  • 77 Lahaye M, Kaeffer B. Seaweed dietary fibres: Structure, physico-chemical and biological properties relevent to intestinal physiology. Sci Aliment 1997; 17: 563-584
  • 78 Cummings JH, Mann JI, Nishida C. et al. Dietary fibre: An agreed definition. Lancet 2009; 373: 365-366
  • 79 Harris RE, Chlebowski RT, Jackson RD. et al. Breast cancer and nonsteroidal anti-inflammatory drugs: Prospective results from the Women's Health Initiative. Cancer Res 2003; 63: 6096-6101
  • 80 Stansbury, Jillian, SEAWEED, CHEWING GUM AND GERD. Ndnr Botanical Medicine, [Online] January 17, 2017. Available from: http://ndnr.com/botanical-medicine/seaweed-chewing-gum-and-gerd/#comments
  • 81 Greene ER, Huang S, Serhan CN. et al. Regulation of inflammation in cancer by eicosanoids. Prostaglandins Other Lipid Mediators 2011; 96: 27-36
  • 82 Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420: 860-867
  • 83 Vakkila J, Lotze MT. Inflammation and necrosis promote tumour growth. Nat Rev Immunol 2004; 4: 641-648
  • 84 Ekbom A, Helmick C, Zack M. et al. Ulcerative colitis and colorectal cancer. N Engl J Med 1990; 323: 1228-1233
  • 85 Kulaylat MN, Dayton MT. Ulcerative colitis and cancer. J Surg Oncol 2010; 101: 706-712
  • 86 Kalitnik AA, Marcov PA, Anastyuk SD. et al. Gelling polysaccharide from Chondrus armatus and its oligosaccharides: The structural peculiarities and anti-inflammatory. Carbohydr Polym 2015; 115: 768-775
  • 87 Sokolova EV, Karetin Y, Davydova VN. et al. Carrageenans effect on neutrophils alone and in combination with LPS in vitro . J Biomed Mater Res Part A 2016; 104: 1603-1609
  • 88 Abdel-Latif MM, Duggan S, Reynolds JV. et al. Inflammation and esophageal carcinogenesis. Curr Opin Pharmacol 2009; 9: 396-404
  • 89 Hardikar S, Onstad L, Song X. et al. Inflammation and oxidative stress markers and esophageal adenocarcinoma incidence in a Barrett's esophagus cohort. Cancer Epidemiol Biomarkers Prev 2014; 23: 2393-2403
  • 90 Wang Q, Hao J, Guan Q. et al. The Mediterranean diet and gastrointestinal cancers risk. Recent Pat Food Nutr Agric 2014; 6: 23-26
  • 91 Jessri M, Rashidkhani B, Hajizadeh B. et al. Adherence to Mediterranean-style dietary pattern and risk of esophageal squamous cell carcinoma: A case-control study in Iran. J Am Coll Nutr 2012; 31: 338-351
  • 92 Caliari SR, Burdick JA. A practical guide to hydrogels for cell culture. Nat Methods 2016; 13: 405-414
  • 93 Rybtsov S, Batsivari A, Bilotkach K. et al. Tracing the origin of the HSC hierarchy reveals an SCF-dependent, IL-3-independent CD43- embryonic precursor. Stem Cell Rep 2014; 3: 489-501
  • 94 Huang Q, Zou Y, Arno MC. et al. Hydrogel scaffolds for differentiation of adipose-derived stem cells. Chem Soc Rev 2017; 46: 6255-6275