Potential use of bacterial pigments as anticancer drugs and female reproductive toxicity: a review

Santos, André Luiz da Conceição; Ferreira, Anna Clara Accioly; Figueiredo, José Ricardo de

doi:10.1590/1809-6891v23e-72911E

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Ciência Animal Brasileira

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Review • Ciênc. anim. bras. 23 • 2022 • https://doi.org/10.1590/1809-6891v23e-72911E copy

Potential use of bacterial pigments as anticancer drugs and female reproductive toxicity: a review

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Natural bioactive compounds obtained from microorganisms, have awakened particular interest in the industry nowadays. This attention comes when natural resources depletion is pronounced, and the acquisition of both new plant origin resources and bioactive products, represents a challenge for the next generations. In this sense, prospecting for large-scale production and use of bacterial pigments is a necessary strategy for the development of novel products. A wide variety of properties have been attributed to these substances and, among them, their therapeutic potential against important diseases, such as cancer. There is consensus that available chemotherapy protocols are known to detrimentally affect cancer patients fertility. Hence, considerable part of the deleterious effects of chemotherapy is related to the drugs cytotoxicity, which, in addition to cancer cells, also affect normal cells. Therefore, the intrinsic properties of bacterial pigments associated with low cytotoxicity and relevant cell selectivity, certified them as potential anticancer drugs. However, little information is available about reproductive toxicity of these new and promising compounds. Thus, the present review aims to address the main bacterial pigments, their potential uses as anticancer drugs and their possible toxic effects, especially on the female gonad.

Keywords:
cancer; chemotherapy; fertility; bioactive compounds; bacteria

Chemotherapy class	Drugs	Mechanism of action	Gonadotoxicity
Alkylating agents	Carboplatin	Prevent cell division by cross-linking DNA strands. Their activity does not depend on DNA synthesis in the target cells. Cyclophosphamide also inhibits DNA synthesis	Induce double strand breaks in oocytes; DNA damage that interferes with transcription and cell replication, leading to oocyte death
	Cisplatin
	Oxaliplatin
	Cyclophosphamide
	Ifosfamide
	Altretamine
Antimetabolites	5-Fluorouracil	Inhibit the metabolic processes necessary for the synthesis of purines, pyrimidines, and nucleic acids	Low gonadotoxic risk
	Methotrexate
	Capecitabine
	Gemcitabine
	Pemetrexed
Antitumor antibiotics	Dactinomycin	Acts via DNA intercalation, interfering with the synthesis of nucleic acids	Positively regulate p53 protein which induces apoptosis; induce DNA double-strand breaks leading to ATM activation, which initiates apoptosis
	Bleomycin
	Doxorubicin
Vinca Alkaloids	Vinblastine	Acts by altering the normal assembly, disassembly and stabilization of microtubules	Low gonadotoxic risk
	Vincristine
	Vinorelbine
Taxanes	Paclitaxel		Low and transient gonadotoxic risk
Taxanes	Docetaxel		Low and transient gonadotoxic risk
Epipodophyllotoxin	Etoposide		Low gonadotoxic risk in non-pregnant women
Epothilone	Ixabepilone		N/A
Camptothecin Analogs	Topotecan	Inhibit topoisomerase I, inducing single-stranded DNA breaks	N/A
	Irinotecan		High gonadotoxic risk when combined with several chemotherapeutic agents

Pigments	Producing bacteria	Pharmacological potential	Anticancer potential
Pigments	Producing bacteria	Pharmacological potential	Cell lineage/Tumor type	Experimental system	Animal model (in vivo)
Carotenoids	Flavobacterium spp., Agrobacterium spp., Micrococcus spp., Pseudomonas aeruginosa, Serratia marcescens, Chromobacterium spp., Rheinheimera spp. e Arthrobacter spp(²¹21 Ram S, Mitra M, Shah F, Tirkey SR, Mishra S. Bacteria as an alternate biofactory for carotenoid production: A review of its applications, opportunities and challenges. J Funct Foods [Internet]. 2020;67:103867. Available from: https://doi.org/10.1016/j.jff.2020.103867 https://doi.org/10.1016/j.jff.2020.10386... )	Antioxidant(⁵²52 Meza-Herrera CA, Vargas-Beltran F, Tena-Sempere M, González-Bulnes A, Macias-Cruz U, Veliz-Deras FG. Short-term betacarotene supplementation positively affects ovarian activity and serum insulin concentrations in a goat model. J Endocrinol Invest. 2013;36(3):185-9. doi: 10.3275/8410 https://doi.org/10.3275/8410... ,⁶¹61 Hix LM, Lockwood SF, Bertram JS. Bioactive carotenoids: Potent antioxidants and regulators of gene expression. Redox Rep. 2004;9(4):181-91. doi: 10.1179/135100004225005967 https://doi.org/10.1179/1351000042250059... ,⁶²62 Grune T, Lietz G, Palou A, Ross AC, Stahl W, Tang G, et al. B-Carotene is am important vitamin a source for humans. J Nutr. 2010;140:2268-85. doi: 10.3945/jn.109.119024 https://doi.org/10.3945/jn.109.119024... ), anti-inflammatory(⁶⁹69 Nagendraprabhu P, Sudhandiran G. Astaxanthin inhibits tumor invasion by decreasing extracellular matrix production and induces apoptosis in experimental rat colon carcinogenesis by modulating the expressions of ERK-2, NFkB and COX-2. Invest New Drugs. 2011;29(2):207-24. doi: 10.1007/s10637-009-9342-5 https://doi.org/10.1007/s10637-009-9342-... ), anticancer(⁶⁸68 Holzapfel NP, Shokoohmand A, Wagner F, Landgraf M, Champ S, Holzapfel BM, et al. Lycopene reduces ovarian tumor growth and intraperitoneal metastatic load. Am J Cancer Res. 2017;7(6):1322-36. 69 Nagendraprabhu P, Sudhandiran G. Astaxanthin inhibits tumor invasion by decreasing extracellular matrix production and induces apoptosis in experimental rat colon carcinogenesis by modulating the expressions of ERK-2, NFkB and COX-2. Invest New Drugs. 2011;29(2):207-24. doi: 10.1007/s10637-009-9342-5 https://doi.org/10.1007/s10637-009-9342-... 70 Takeshima M, Ono M, Higuchi T, Chen C, Hara T, Nakano S. Anti-proliferative and apoptosis-inducing activity of lycopene against three subtypes of human breast cancer cell lines. Cancer Sci. 2014;105(3):252-7. doi: 10.1111/cas.12349 https://doi.org/10.1111/cas.12349... -⁷¹71 Jeong Y, Lim JW, Kim H. Lycopene inhibits reactive oxugen species-mediated nf-kb signaling and induces apoptosis in pancreatic cancer cells. Nutrients. 2019;11(4):1-17. doi: doi:10.3390/nu11040762 https://doi.org/10.3390/nu11040762... )	OV-MZ-6 ovarian cancer cells(⁶⁸68 Holzapfel NP, Shokoohmand A, Wagner F, Landgraf M, Champ S, Holzapfel BM, et al. Lycopene reduces ovarian tumor growth and intraperitoneal metastatic load. Am J Cancer Res. 2017;7(6):1322-36.), MDA-MB-468 breast cancer cells(⁷⁰70 Takeshima M, Ono M, Higuchi T, Chen C, Hara T, Nakano S. Anti-proliferative and apoptosis-inducing activity of lycopene against three subtypes of human breast cancer cell lines. Cancer Sci. 2014;105(3):252-7. doi: 10.1111/cas.12349 https://doi.org/10.1111/cas.12349... ), Panc-1 pancreatic cancer cells(⁷¹71 Jeong Y, Lim JW, Kim H. Lycopene inhibits reactive oxugen species-mediated nf-kb signaling and induces apoptosis in pancreatic cancer cells. Nutrients. 2019;11(4):1-17. doi: doi:10.3390/nu11040762 https://doi.org/10.3390/nu11040762... )	In vitro and in vivo	Murine
Prodiginines	Serratia marcescens(⁸⁴84 Liu Y, Zhou H, Ma X, Lin C, Lu L, Liu D, et al. Prodigiosin inhibits proliferation, migration, and invasion of nasopharyngeal cancer cells. Cell Physiol Biochem. 2018;48(4):1556-62. doi: 10.1159/00049227 https://doi.org/10.1159/00049227... ), Hahella chejuensis, Pseudomonas magnesiorubra, Vibrio spp., Streptomyces spp, Streptoverticillium rubrireticuli, Actinomadura madurae, Saccharopolyspora sp., Actinomadura pelletieri, Alteromonas rubra, Pseudoalteromonas denitrificans e Hahella chejuensis(⁸³83 Elahian F, Moghimi B, Dinmohammadi F, Ghamghami M, Hamidi M, Mirzaei SA. The anticancer agent prodigiosin is not a multidrug resistance protein substrate. DNA Cell Biol. 2013;32(3):90-7. doi: 10.1089/dna.2012.1902 https://doi.org/10.1089/dna.2012.1902... ,⁸⁶86 Gulani C, Bhattacharya S, Das A. Assessment of process parameters influencing the enhanced production of prodigiosin from Serratia marcescens and evaluation of its antimicrobial, antioxidant and dyeing potentials. Malays J Microbiol. 2012;8(2):116-22. doi: 10.21161/mjm.03612 https://doi.org/10.21161/mjm.03612... )	Antiviral(⁹¹91 Suryawanshi RK, Koujah L, Patil CD, Ames JM, Agelidis A, Yadavalli T, et al. Bacterial pigment prodigiosin demonstrates a unique antiherpesvirus activity that is mediated through inhibition of prosurvival signal transducers. J Virol. 2020;94(13):1-30. doi: 10.1128/JVI.00251-20 https://doi.org/10.1128/JVI.00251-20... ), antibacterial, antifungal (⁹²92 Suryawanshi RK, Patil CD, Koli SH, Hallsworth JE, Patil S V. Antimicrobial activity of prodigiosin is attributable to plasma-membrane damage. Nat Prod Res [Internet]. 2017;31(5):572-7. Available from: http://dx.doi.org/10.1080/14786419.2016.1195380 http://dx.doi.org/10.1080/14786419.2016.... ), anti-inflammatory(⁹³93 Krishna PS, Vani K, Prasad MR, Samatha B, Hima Bindu NSVSL, Singara Charya MA, et al. In -silico molecular docking analysis of prodigiosin and cycloprodigiosin as COX-2 inhibitors. Springerplus. 2013;2(1):1-6. http://www.springerplus.com/content/2/1/172 http://www.springerplus.com/content/2/1/... ), antioxidant(⁸⁷87 Sudhakar C, Shobana C, Selvankumar T, Selvam K. Prodigiosin production from Serratia marcescens strain CSK and their antioxidant, antibacterial, cytotoxic effect and in silico study of caspase-3 apoptotic protein. Biotechnol Appl Biochem. 2021;1-14. doi: 10.1002/bab.2261 https://doi.org/10.1002/bab.2261... ), anticancer(¹⁵15 Anwar MM, Shalaby M, Embaby AM, Saeed H, Agwa MM, Hussein A. Prodigiosin/PU-H71 as a novel potential combined therapy for triple negative breast cancer (TNBC): preclinical insights. Sci Rep [Internet]. 2020;10(1):1-15. Available from: https://doi.org/10.1038/s41598-020-71157-w https://doi.org/10.1038/s41598-020-71157... ,⁸⁹89 Ji S, Sun R, Xu K, Man Z, Ji J, Pu Y, et al. Prodigiosin induces apoptosis and inhibits autophagy via the extracellular signal-regulated kinase pathway in K562 cells. Toxicol Vitr [Internet]. 2019;60(11):107-15. Available from: https://doi.org/10.1016/j.tiv.2019.05.003 https://doi.org/10.1016/j.tiv.2019.05.00... ,⁹⁴94 Montaner B, Navarro S, Piqué M, Vilaseca M, Martinell M, Giralt E, et al. Prodigiosin from the supernatant of Serratia marcescens induces apoptosis in haematopoietic cancer cell lines. Br J Pharmacol. 2000;131(3):585-93. doi: 10.1038/sj.bjp.0703614 https://doi.org/10.1038/sj.bjp.0703614... 95 Lapenda JCL, Alves VP, Adam ML, Rodrigues MD, Nascimento SC. Cytotoxic effect of prodigiosin, natural red pigment, isolated from Serratia marcescens UFPEDA 398. Indian J Microbiol [Internet]. 2020;60(2):182-95. Available from: https://doi.org/10.1007/s12088-020-00859-6 https://doi.org/10.1007/s12088-020-00859... -⁹⁶96 Lin P Bin, Shen J, Ou PY, Liu LY, Chen ZY, Chu FJ, et al. Prodigiosin isolated from Serratia marcescens in the Periplaneta americana gut and its apoptosis‑inducing activity in HeLa cells. Oncol Rep. 2019;41(6):3377-85. doi: 10.3892/or.2019.7089 https://doi.org/10.3892/or.2019.7089... )	K562 leukemia cells(⁸⁹89 Ji S, Sun R, Xu K, Man Z, Ji J, Pu Y, et al. Prodigiosin induces apoptosis and inhibits autophagy via the extracellular signal-regulated kinase pathway in K562 cells. Toxicol Vitr [Internet]. 2019;60(11):107-15. Available from: https://doi.org/10.1016/j.tiv.2019.05.003 https://doi.org/10.1016/j.tiv.2019.05.00... ), Jurkat cells, NOS, HL-60, RAMOS of hematopoietic cancer(⁹⁴94 Montaner B, Navarro S, Piqué M, Vilaseca M, Martinell M, Giralt E, et al. Prodigiosin from the supernatant of Serratia marcescens induces apoptosis in haematopoietic cancer cell lines. Br J Pharmacol. 2000;131(3):585-93. doi: 10.1038/sj.bjp.0703614 https://doi.org/10.1038/sj.bjp.0703614... ), NCHI-292 lung carcinoma cells, HEP-2 cells of laryngeal carcinoma, MCF-7 breast cancer cells(⁹⁵95 Lapenda JCL, Alves VP, Adam ML, Rodrigues MD, Nascimento SC. Cytotoxic effect of prodigiosin, natural red pigment, isolated from Serratia marcescens UFPEDA 398. Indian J Microbiol [Internet]. 2020;60(2):182-95. Available from: https://doi.org/10.1007/s12088-020-00859-6 https://doi.org/10.1007/s12088-020-00859... ), HeLa cells from cervical cancer(⁹⁶96 Lin P Bin, Shen J, Ou PY, Liu LY, Chen ZY, Chu FJ, et al. Prodigiosin isolated from Serratia marcescens in the Periplaneta americana gut and its apoptosis‑inducing activity in HeLa cells. Oncol Rep. 2019;41(6):3377-85. doi: 10.3892/or.2019.7089 https://doi.org/10.3892/or.2019.7089... ), MDA-MB-231 breast adenocarcinoma cells(¹⁵15 Anwar MM, Shalaby M, Embaby AM, Saeed H, Agwa MM, Hussein A. Prodigiosin/PU-H71 as a novel potential combined therapy for triple negative breast cancer (TNBC): preclinical insights. Sci Rep [Internet]. 2020;10(1):1-15. Available from: https://doi.org/10.1038/s41598-020-71157-w https://doi.org/10.1038/s41598-020-71157... )	In vitro	N/A
Pyocyanin	Pseudomonas aeruginosa (⁹⁸98 Ashour EA, Farsi RM, Alaidaroos BA, Abdel-Moneim AME, El-Saadony MT, Osman AO, et al. Impacts of dietary supplementation of pyocyanin powder on growth performance, carcase traits, blood chemistry, meat quality and gut microbial activity of broilers. Ital J Anim Sci [Internet]. 2021;20(1):1357-72. Available from: https://doi.org/10.1080/1828051X.2021.1924087 https://doi.org/10.1080/1828051X.2021.19... ,¹⁰³103 Laxmi M, Bhat SG. Characterization of pyocyanin with radical scavenging and antibiofilm properties isolated from Pseudomonas aeruginosa strain BTRY1. 3 Biotech. 2016;6(1):1-5. doi: 10.1007/s13205-015-0350-1 https://doi.org/10.1007/s13205-015-0350-... )	Antibacterial(¹⁰³103 Laxmi M, Bhat SG. Characterization of pyocyanin with radical scavenging and antibiofilm properties isolated from Pseudomonas aeruginosa strain BTRY1. 3 Biotech. 2016;6(1):1-5. doi: 10.1007/s13205-015-0350-1 https://doi.org/10.1007/s13205-015-0350-... ), pro-oxidant(¹⁷17 Marrez DA, Mohamad HS. Biological activity and applications of pyocyanin produced by Pseudomonas aeruginosa. Open Access J Biomed Sci. 2020;1(4):140-4. doi: 10.38125/OAJBS.000133 https://doi.org/10.38125/OAJBS.000133... ), antifungal(⁹⁸98 Ashour EA, Farsi RM, Alaidaroos BA, Abdel-Moneim AME, El-Saadony MT, Osman AO, et al. Impacts of dietary supplementation of pyocyanin powder on growth performance, carcase traits, blood chemistry, meat quality and gut microbial activity of broilers. Ital J Anim Sci [Internet]. 2021;20(1):1357-72. Available from: https://doi.org/10.1080/1828051X.2021.1924087 https://doi.org/10.1080/1828051X.2021.19... ), anticancer(⁹⁹99 Moayedi A, Nowroozi J, Akhavan Sepahy A. Cytotoxic effect of pyocyanin on human pancreatic cancer cell line (Panc-1). Iran J Basic Med Sci. 2018;21(8):794-9. doi: 10.22038/IJBMS.2018.27865.6799 https://doi.org/10.22038/IJBMS.2018.2786... ,¹⁰⁴104 Zhao J, Wu Y, Alfred AT, Wei P, Yang S. Anticancer effects of pyocyanin on HepG2 human hepatoma cells. Lett Appl Microbiol. 2014;58:541-8. doi: 10.1111/lam.12224 https://doi.org/10.1111/lam.12224... -¹⁰⁵105 Muller M. Premature cellular senescence induced by pyocyanin, a redox-active Pseudomonas aeruginosa toxin. Free Radic Biol Med. 2006;41(11):1670-7. doi: 10.1016/j.freeradbiomed.2006.09.004 https://doi.org/10.1016/j.freeradbiomed.... )	HepG2 hepatocellular carcinoma cells(¹⁰⁴104 Zhao J, Wu Y, Alfred AT, Wei P, Yang S. Anticancer effects of pyocyanin on HepG2 human hepatoma cells. Lett Appl Microbiol. 2014;58:541-8. doi: 10.1111/lam.12224 https://doi.org/10.1111/lam.12224... ), Panc-1 pancreatic cancer cells(⁹⁹99 Moayedi A, Nowroozi J, Akhavan Sepahy A. Cytotoxic effect of pyocyanin on human pancreatic cancer cell line (Panc-1). Iran J Basic Med Sci. 2018;21(8):794-9. doi: 10.22038/IJBMS.2018.27865.6799 https://doi.org/10.22038/IJBMS.2018.2786... )	In vitro	N/A
Melanin	Streptomyces glaucescen(⁴⁶46 El-Naggar N, El-Ewasy SM. Bioproduction, characterization, anticancer and antioxidant activities of extracellular melanin pigment produced by newly isolated microbial cell factories Streptomyces glauscescens NEAE-H. Sci Rep. 2017;7:1-19. doi: 10.1038/srep42129 https://doi.org/10.1038/srep42129... ), Bacillus licheniformis(⁷⁴74 Gamal Shalaby AS, Ragab TIM, Helal MMI, Esawy MA. Optimization of Bacillus licheniformis MAL tyrosinase: in vitro anticancer activity for brown and black eumelanin. Heliyon [Internet]. 2019;5(5):e01657. Available from: https://doi.org/10.1016/j.heliyon.2019.e01657 https://doi.org/10.1016/j.heliyon.2019.e... ), Pseudomonas aeruginosa(⁴⁸48 Pavan ME, López NI, Pettinari MJ. Melanin biosynthesis in bacteria, regulation and production perspectives. Appl Microbiol Biotechnol. 2020;104(4):1357-70. doi: 10.1007/s00253-019-10245-y https://doi.org/10.1007/s00253-019-10245... ), Burkholderia xenovorans, Legionella pneumophila(⁷³73 Singh S, Nimse SB, Mathew DE, Dhimmar A, Sahastrabudhe H, Gajjar A, et al. Microbial melanin: Recent advances in biosynthesis, extraction, characterization, and applications. Biotechnol Adv [Internet]. 2021;53(5):107773. Available from: https://doi.org/10.1016/j.biotechadv.2021.107773 https://doi.org/10.1016/j.biotechadv.202... )	Antioxidant(⁴⁶46 El-Naggar N, El-Ewasy SM. Bioproduction, characterization, anticancer and antioxidant activities of extracellular melanin pigment produced by newly isolated microbial cell factories Streptomyces glauscescens NEAE-H. Sci Rep. 2017;7:1-19. doi: 10.1038/srep42129 https://doi.org/10.1038/srep42129... ,⁴⁸48 Pavan ME, López NI, Pettinari MJ. Melanin biosynthesis in bacteria, regulation and production perspectives. Appl Microbiol Biotechnol. 2020;104(4):1357-70. doi: 10.1007/s00253-019-10245-y https://doi.org/10.1007/s00253-019-10245... ), anticancer(⁴⁶46 El-Naggar N, El-Ewasy SM. Bioproduction, characterization, anticancer and antioxidant activities of extracellular melanin pigment produced by newly isolated microbial cell factories Streptomyces glauscescens NEAE-H. Sci Rep. 2017;7:1-19. doi: 10.1038/srep42129 https://doi.org/10.1038/srep42129... -⁴⁷47 Arun G, Eyini M, Gunasekaran P. Characterization and biological activities of extracellular melanin produced by Schizophyllum commune (Fries). Indian J Exp Biol. 2015;53(6):380-7.,⁷⁴74 Gamal Shalaby AS, Ragab TIM, Helal MMI, Esawy MA. Optimization of Bacillus licheniformis MAL tyrosinase: in vitro anticancer activity for brown and black eumelanin. Heliyon [Internet]. 2019;5(5):e01657. Available from: https://doi.org/10.1016/j.heliyon.2019.e01657 https://doi.org/10.1016/j.heliyon.2019.e... )	HEP-2 cells of laryngeal carcinoma(⁴⁷47 Arun G, Eyini M, Gunasekaran P. Characterization and biological activities of extracellular melanin produced by Schizophyllum commune (Fries). Indian J Exp Biol. 2015;53(6):380-7.), HFB4 skin cancer cells(⁴⁶46 El-Naggar N, El-Ewasy SM. Bioproduction, characterization, anticancer and antioxidant activities of extracellular melanin pigment produced by newly isolated microbial cell factories Streptomyces glauscescens NEAE-H. Sci Rep. 2017;7:1-19. doi: 10.1038/srep42129 https://doi.org/10.1038/srep42129... ), MCF-7 breast cancer cells, HepG2 hepatocellular carcinoma cells, HCT116 colon cancer cells(⁷⁴74 Gamal Shalaby AS, Ragab TIM, Helal MMI, Esawy MA. Optimization of Bacillus licheniformis MAL tyrosinase: in vitro anticancer activity for brown and black eumelanin. Heliyon [Internet]. 2019;5(5):e01657. Available from: https://doi.org/10.1016/j.heliyon.2019.e01657 https://doi.org/10.1016/j.heliyon.2019.e... )	In vitro	N/A
Violacein	Chromobacterium violaceum(⁷⁵75 Matz C., Deines P, Boenigk J, Arndt H, Eberl L, Kjelleberg S, Ju¨rgens. Impact of violacein-producing bacteria on survival and feeding of bacterivorous nanoflagellates. Appl Environ Microbiol. 2004;70(3): 1593-9. doi: 10.1128/AEM.70.3.1593-1599.2004 https://doi.org/10.1128/AEM.70.3.1593-15... ), Janthinobacterium lividum(⁸⁰80 Masuelli L, Pantanella F, La Regina G, Benvenuto M, Fantini M, Mattera R, et al. Violacein, an indole-derived purple-colored natural pigment produced by Janthinobacterium lividum, inhibits the growth of head and neck carcinoma cell lines both in vitro and in vivo. Tumor Biol. 2016;37(3):3705-17. doi: 10.1007/s13277-015-4207-3 https://doi.org/10.1007/s13277-015-4207-... )	Antibacterial(⁷⁶76 Dodou HV., de Morais Batista AH, Sales GWP, de Medeiros SC, Rodrigues ML, Nogueira PCN, et al. Violacein antimicrobial activity on Staphylococcus epidermidis and synergistic effect on commercially available antibiotics. J Appl Microbiol. 2017;123(4):853-60. doi: 10.1111/jam.13547 https://doi.org/10.1111/jam.13547... ), antiviral(⁷⁷77 Andrighetti-Fröhner CR, Antonio R V, Creczynski-Pasa TB, Barardi CRM, Simões CMO. Cytotoxicity and potential antiviral evaluation of violacein produced by Chromobacterium violaceum. Mem Inst Oswaldo Cruz. 2003;98(6):843-8. doi: 10.1590/s0074-02762003000600023 https://doi.org/10.1590/s0074-0276200300... ), antiprotozoal(⁷⁵75 Matz C., Deines P, Boenigk J, Arndt H, Eberl L, Kjelleberg S, Ju¨rgens. Impact of violacein-producing bacteria on survival and feeding of bacterivorous nanoflagellates. Appl Environ Microbiol. 2004;70(3): 1593-9. doi: 10.1128/AEM.70.3.1593-1599.2004 https://doi.org/10.1128/AEM.70.3.1593-15... ), antioxidant(⁴⁴44 Bromberg N, Dreyfuss JL, Regatieri C V., Palladino M V., Durán N, Nader HB, et al. Growth inhibition and pro-apoptotic activity of violacein in Ehrlich ascites tumor. Chem Biol Interact. 2010;186(1):43-52. doi: 10.1016/j.cbi.2010.04.016 https://doi.org/10.1016/j.cbi.2010.04.01... ), anticancer(⁴⁴44 Bromberg N, Dreyfuss JL, Regatieri C V., Palladino M V., Durán N, Nader HB, et al. Growth inhibition and pro-apoptotic activity of violacein in Ehrlich ascites tumor. Chem Biol Interact. 2010;186(1):43-52. doi: 10.1016/j.cbi.2010.04.016 https://doi.org/10.1016/j.cbi.2010.04.01... -⁴⁵45 Kodach LL, Bos CL, Durán N, Peppelenbosch MP, Ferreira C V., Hardwick JCH. Violacein synergistically increases 5-fluorouracil cytotoxicity, induces apoptosis and inhibits Akt-mediated signal transduction in human colorectal cancer cells. Carcinogenesis. 2006;27(3):508-16. doi: 10.1093/carcin/bgi307 https://doi.org/10.1093/carcin/bgi307... , ⁷⁸78 Ferreira CV, Bos CL, Versteeg HH, Justo GZ, Durán N, Peppelenbosch MP. Molecular mechanism of violacein-mediated human leukemia cell death. Blood. 2004;104(5):1459-64. doi: 10.1182/blood-2004-02-0594 https://doi.org/10.1182/blood-2004-02-05... 79 Carvalho DD, Costa FTM, Duran N, Haun M. Cytotoxic activity of violacein in human colon cancer cells. Toxicol Vitr. 2006;20(8):1514-21. doi: 10.1016/j.tiv.2006.06.007 https://doi.org/10.1016/j.tiv.2006.06.00... 80 Masuelli L, Pantanella F, La Regina G, Benvenuto M, Fantini M, Mattera R, et al. Violacein, an indole-derived purple-colored natural pigment produced by Janthinobacterium lividum, inhibits the growth of head and neck carcinoma cell lines both in vitro and in vivo. Tumor Biol. 2016;37(3):3705-17. doi: 10.1007/s13277-015-4207-3 https://doi.org/10.1007/s13277-015-4207-... -⁸¹81 Mehta T, Vercruysse K, Johnson T, Ejiofor AO, Myles E, Quick QA. Violacein induces p44/42 mitogen-activated protein kinase-mediated solid tumor cell death and inhibits tumor cell migration. Mol Med Rep. 2015;12(1):1443-8. doi: 10.3892/mmr.2015.3525 https://doi.org/10.3892/mmr.2015.3525... )	Ehrlich tumor cells(⁴⁴44 Bromberg N, Dreyfuss JL, Regatieri C V., Palladino M V., Durán N, Nader HB, et al. Growth inhibition and pro-apoptotic activity of violacein in Ehrlich ascites tumor. Chem Biol Interact. 2010;186(1):43-52. doi: 10.1016/j.cbi.2010.04.016 https://doi.org/10.1016/j.cbi.2010.04.01... ), HL-60 leukemia cells(⁷⁸78 Ferreira CV, Bos CL, Versteeg HH, Justo GZ, Durán N, Peppelenbosch MP. Molecular mechanism of violacein-mediated human leukemia cell death. Blood. 2004;104(5):1459-64. doi: 10.1182/blood-2004-02-0594 https://doi.org/10.1182/blood-2004-02-05... ), Caco-2 colon cancer cells(⁷⁹79 Carvalho DD, Costa FTM, Duran N, Haun M. Cytotoxic activity of violacein in human colon cancer cells. Toxicol Vitr. 2006;20(8):1514-21. doi: 10.1016/j.tiv.2006.06.007 https://doi.org/10.1016/j.tiv.2006.06.00... ), CAL-27 tongue carcinoma cells, FaDu pharyngeal carcinoma cells(⁸⁰80 Masuelli L, Pantanella F, La Regina G, Benvenuto M, Fantini M, Mattera R, et al. Violacein, an indole-derived purple-colored natural pigment produced by Janthinobacterium lividum, inhibits the growth of head and neck carcinoma cell lines both in vitro and in vivo. Tumor Biol. 2016;37(3):3705-17. doi: 10.1007/s13277-015-4207-3 https://doi.org/10.1007/s13277-015-4207-... ), U87 brain tumor cells(⁸¹81 Mehta T, Vercruysse K, Johnson T, Ejiofor AO, Myles E, Quick QA. Violacein induces p44/42 mitogen-activated protein kinase-mediated solid tumor cell death and inhibits tumor cell migration. Mol Med Rep. 2015;12(1):1443-8. doi: 10.3892/mmr.2015.3525 https://doi.org/10.3892/mmr.2015.3525... ), HCT116 colon cancer cells(⁴⁵45 Kodach LL, Bos CL, Durán N, Peppelenbosch MP, Ferreira C V., Hardwick JCH. Violacein synergistically increases 5-fluorouracil cytotoxicity, induces apoptosis and inhibits Akt-mediated signal transduction in human colorectal cancer cells. Carcinogenesis. 2006;27(3):508-16. doi: 10.1093/carcin/bgi307 https://doi.org/10.1093/carcin/bgi307... )	In vitro and in vivo	Murine

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