The impact of low-dose carcinogens and environmental disruptors on tissue invasion and metastasis

Josiah Ochieng¹, Gladys N Nangami¹, Olugbemiga Ogunkua¹, Isabelle R Miousse², Igor Koturbash², Valerie Odero-Marah³, Lisa J McCawley⁴, Pratima Nangia-Makker⁵, Nuzhat Ahmed⁶, Yunus Luqmani⁷, Zhenbang Chen¹, Silvana Papagerakis⁸, Gregory T Wolf⁸, Chenfang Dong⁹, Binhua P Zhou⁹, Dustin G Brown¹⁰, Anna Maria Colacci¹¹, Roslida A Hamid¹², Chiara Mondello¹³, Jayadev Raju¹⁴, Elizabeth P Ryan¹⁰, Jordan Woodrick¹⁵, A Ivana Scovassi¹³, Neetu Singh¹⁶, Monica Vaccari¹¹, Rabindra Roy¹⁵, Stefano Forte¹⁷, Lorenzo Memeo¹⁷, Hosni K Salem¹⁸, Amedeo Amedei¹⁹, Rabeah Al-Temaimi⁷, Fahd Al-Mulla⁷, William H Bisson²⁰, Sakina E Eltom¹

Affiliations

¹ Department of Biochemistry and Cancer Biology, Meharry Medical College, Nashville, TN 37208, USA, Department of Environmental and Occupational Health, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA, Department of Biology/Center for Cancer Research and Therapeutic Development, Clark Atlanta University, Atlanta, GA 30314, USA, Department of Cancer Biology, Vanderbilt University, Nashville, TN 37232, USA, Department of Pathology, Wayne State University, Detroit, MI 48201, USA, Department of Obstetrics and Gynecology, University of Melbourne, Melbourne, Victoria, Australia, Faculty of Pharmacy, Department of Pathology, Kuwait University, Safat 13110, Kuwait, Department of Otolaryngology, University of Michigan Medical College, Ann Arbor, MI 48109, USA, Department of Molecular & Cellular Biochemistry, University of Kentucky, Lexington, KY 40506, USA, Department of Environmental and Radiological Health Sciences/Food Science and Human Nutrition, College of Veterinary Medicine and Biomedical Sciences, Colorado State University/Colorado School of Public Health, Fort Collins, CO 80523-1680, USA, Center for Environmental Carcinogenesis and Risk Assessment, Environmental Protection and Health Prevention Agency, Bologna 40126, Italy, Faculty of Medicine and Health Sciences, University Putra, Serdang, Selangor 43400, Malaysia, Istituto di Genetica Molecolare, CNR, via Abbiategrasso 207, 27100 Pavia, Italy, Toxicology Research Division, Bureau of Chemical Safety Food Directorate, Health Products and Food Branch Health Canada, Ottawa, Ontario K1A0K9, Canada, Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057, USA, Centre for Advanced Research, King George's Medical University, Chowk, Lucknow, Uttar Pradesh 226003, India, Mediterranean Institute of Oncology, Viagrande 95029, Italy, Urology Department, kasr Al-Ainy School of Medicine, Cairo University, El Manial, Cairo 12515, Egypt, Department of Experimental and
² Department of Environmental and Occupational Health, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA.
³ Department of Biology/Center for Cancer Research and Therapeutic Development, Clark Atlanta University, Atlanta, GA 30314, USA.
⁴ Department of Cancer Biology, Vanderbilt University, Nashville, TN 37232, USA.
⁵ Department of Pathology, Wayne State University, Detroit, MI 48201, USA.
⁶ Department of Obstetrics and Gynecology, University of Melbourne, Melbourne, Victoria, Australia.
⁷ Faculty of Pharmacy, Department of Pathology, Kuwait University, Safat 13110, Kuwait.
⁸ Department of Otolaryngology, University of Michigan Medical College, Ann Arbor, MI 48109, USA.
⁹ Department of Molecular & Cellular Biochemistry, University of Kentucky, Lexington, KY 40506, USA.
¹⁰ Department of Environmental and Radiological Health Sciences/Food Science and Human Nutrition, College of Veterinary Medicine and Biomedical Sciences, Colorado State University/Colorado School of Public Health, Fort Collins, CO 80523-1680, USA.
¹¹ Center for Environmental Carcinogenesis and Risk Assessment, Environmental Protection and Health Prevention Agency, Bologna 40126, Italy.
¹² Faculty of Medicine and Health Sciences, University Putra, Serdang, Selangor 43400, Malaysia.
¹³ Istituto di Genetica Molecolare, CNR, via Abbiategrasso 207, 27100 Pavia, Italy.
¹⁴ Toxicology Research Division, Bureau of Chemical Safety Food Directorate, Health Products and Food Branch Health Canada, Ottawa, Ontario K1A0K9, Canada.
¹⁵ Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057, USA.
¹⁶ Centre for Advanced Research, King George's Medical University, Chowk, Lucknow, Uttar Pradesh 226003, India.
¹⁷ Mediterranean Institute of Oncology, Viagrande 95029, Italy.
¹⁸ Urology Department, kasr Al-Ainy School of Medicine, Cairo University, El Manial, Cairo 12515, Egypt.
¹⁹ Department of Experimental and Clinical Medicine, University of Firenze, Firenze 50134, Italy and.
²⁰ Environmental and Molecular Toxicology, Environmental Health Sciences Center, Oregon State University, Corvallis, OR 97331, USA.

PMID: 26106135
PMCID: PMC4565611
DOI: 10.1093/carcin/bgv034

Review

The impact of low-dose carcinogens and environmental disruptors on tissue invasion and metastasis

Josiah Ochieng et al. Carcinogenesis. 2015 Jun.

. 2015 Jun;36 Suppl 1(Suppl 1):S128-59.

doi: 10.1093/carcin/bgv034.

Authors

Affiliations

¹ Department of Biochemistry and Cancer Biology, Meharry Medical College, Nashville, TN 37208, USA, Department of Environmental and Occupational Health, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA, Department of Biology/Center for Cancer Research and Therapeutic Development, Clark Atlanta University, Atlanta, GA 30314, USA, Department of Cancer Biology, Vanderbilt University, Nashville, TN 37232, USA, Department of Pathology, Wayne State University, Detroit, MI 48201, USA, Department of Obstetrics and Gynecology, University of Melbourne, Melbourne, Victoria, Australia, Faculty of Pharmacy, Department of Pathology, Kuwait University, Safat 13110, Kuwait, Department of Otolaryngology, University of Michigan Medical College, Ann Arbor, MI 48109, USA, Department of Molecular & Cellular Biochemistry, University of Kentucky, Lexington, KY 40506, USA, Department of Environmental and Radiological Health Sciences/Food Science and Human Nutrition, College of Veterinary Medicine and Biomedical Sciences, Colorado State University/Colorado School of Public Health, Fort Collins, CO 80523-1680, USA, Center for Environmental Carcinogenesis and Risk Assessment, Environmental Protection and Health Prevention Agency, Bologna 40126, Italy, Faculty of Medicine and Health Sciences, University Putra, Serdang, Selangor 43400, Malaysia, Istituto di Genetica Molecolare, CNR, via Abbiategrasso 207, 27100 Pavia, Italy, Toxicology Research Division, Bureau of Chemical Safety Food Directorate, Health Products and Food Branch Health Canada, Ottawa, Ontario K1A0K9, Canada, Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057, USA, Centre for Advanced Research, King George's Medical University, Chowk, Lucknow, Uttar Pradesh 226003, India, Mediterranean Institute of Oncology, Viagrande 95029, Italy, Urology Department, kasr Al-Ainy School of Medicine, Cairo University, El Manial, Cairo 12515, Egypt, Department of Experimental and
² Department of Environmental and Occupational Health, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA.
³ Department of Biology/Center for Cancer Research and Therapeutic Development, Clark Atlanta University, Atlanta, GA 30314, USA.
⁴ Department of Cancer Biology, Vanderbilt University, Nashville, TN 37232, USA.
⁵ Department of Pathology, Wayne State University, Detroit, MI 48201, USA.
⁶ Department of Obstetrics and Gynecology, University of Melbourne, Melbourne, Victoria, Australia.
⁷ Faculty of Pharmacy, Department of Pathology, Kuwait University, Safat 13110, Kuwait.
⁸ Department of Otolaryngology, University of Michigan Medical College, Ann Arbor, MI 48109, USA.
⁹ Department of Molecular & Cellular Biochemistry, University of Kentucky, Lexington, KY 40506, USA.
¹⁰ Department of Environmental and Radiological Health Sciences/Food Science and Human Nutrition, College of Veterinary Medicine and Biomedical Sciences, Colorado State University/Colorado School of Public Health, Fort Collins, CO 80523-1680, USA.
¹¹ Center for Environmental Carcinogenesis and Risk Assessment, Environmental Protection and Health Prevention Agency, Bologna 40126, Italy.
¹² Faculty of Medicine and Health Sciences, University Putra, Serdang, Selangor 43400, Malaysia.
¹³ Istituto di Genetica Molecolare, CNR, via Abbiategrasso 207, 27100 Pavia, Italy.
¹⁴ Toxicology Research Division, Bureau of Chemical Safety Food Directorate, Health Products and Food Branch Health Canada, Ottawa, Ontario K1A0K9, Canada.
¹⁵ Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC 20057, USA.
¹⁶ Centre for Advanced Research, King George's Medical University, Chowk, Lucknow, Uttar Pradesh 226003, India.
¹⁷ Mediterranean Institute of Oncology, Viagrande 95029, Italy.
¹⁸ Urology Department, kasr Al-Ainy School of Medicine, Cairo University, El Manial, Cairo 12515, Egypt.
¹⁹ Department of Experimental and Clinical Medicine, University of Firenze, Firenze 50134, Italy and.
²⁰ Environmental and Molecular Toxicology, Environmental Health Sciences Center, Oregon State University, Corvallis, OR 97331, USA.

PMID: 26106135
PMCID: PMC4565611
DOI: 10.1093/carcin/bgv034

Abstract

The purpose of this review is to stimulate new ideas regarding low-dose environmental mixtures and carcinogens and their potential to promote invasion and metastasis. Whereas a number of chapters in this review are devoted to the role of low-dose environmental mixtures and carcinogens in the promotion of invasion and metastasis in specific tumors such as breast and prostate, the overarching theme is the role of low-dose carcinogens in the progression of cancer stem cells. It is becoming clearer that cancer stem cells in a tumor are the ones that assume invasive properties and colonize distant organs. Therefore, low-dose contaminants that trigger epithelial-mesenchymal transition, for example, in these cells are of particular interest in this review. This we hope will lead to the collaboration between scientists who have dedicated their professional life to the study of carcinogens and those whose interests are exclusively in the arena of tissue invasion and metastasis.

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Figures

**Figure 1.**
Key steps of invasion and metastasis.

**Figure 2.**
Tissue invasion and metastatic pathways influenced by group 1 carcinogens.

**Figure 3.**
Modulation of cancer stem cells and epithelial plasticity by low dose environmental carcinogens.

**Fig. 4.**
Potential impact of environmental disruptors on the key pathways of tissue invasion and metastasis. The disruptive pathways supported by experimental evidence are denoted by +, whereas those for which there are no strong experimental evidence are denoted by ? +.

See this image and copyright information in PMC

References

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1. Klymkowsky M.W., et al. (2009) Epithelial-mesenchymal transition: a cancer researcher’s conceptual friend and foe. Am. J. Pathol., 174, 1588–1593. - PMC - PubMed
1. Ding S.Z., et al. (2013) Epithelial-mesenchymal transition during oncogenic transformation induced by hexavalent chromium involves reactive oxygen species-dependent mechanism in lung epithelial cells. Toxicol. Appl. Pharmacol., 269, 61–71. - PMC - PubMed

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The impact of low-dose carcinogens and environmental disruptors on tissue invasion and metastasis

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The impact of low-dose carcinogens and environmental disruptors on tissue invasion and metastasis

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