Antiproliferative Effect on Cancer Cells of Novel Pink Red-like Pigments and Derivatives Produced by Streptomyces coelicoflavus Strains

Assia Mouslim¹, Saad Menggad², Norddine Habti³, El Bachir Affar² and Mohammed Menggad^1,

¹Laboratory of Physiopathology and Molecular Genetics, Faculty of Sciences Ben M'Sik, Hassan II University of Casablanca, Morocco

²MRH Research Center, Department of Medicine, University of Montréal, Canada

³Laboratory of Haematology, Cellular and Genetic Engineering, Faculty of medicine and pharmacy, Hassan II University of Casablanca, Morocco

Cite this paper:
Assia Mouslim, Saad Menggad, Norddine Habti, El Bachir Affar and Mohammed Menggad. Antiproliferative Effect on Cancer Cells of Novel Pink Red-like Pigments and Derivatives Produced by Streptomyces coelicoflavus Strains. Journal of Cancer Research and Treatment. 2019; 7(1):27-33. doi: 10.12691/jcrt-7-1-5

Abstract

Pink red-like pigments of crud extracts produced by Streptomyces coelicoflavus MFB11, MFB20, MFB21, MFB23 and MFB24 strains and variants from two spontaneous mutants (MFB11-V and MFB11-Y) as well as prepared fractions (FA and FB) from MFB21 and MFB24 strain pigments were screened for antiproliferative effect by MTT. Cancer cell targets used in this screening were P3 Mice myeloid cell line and/or U2OS human osteosarcoma cell line. The results showed an important antiproliferative effect of some strain pigments on the two organism cell types. U2OS human osteosarcoma cell line was more sensitive to the pigments and showed different antiproliferative effect profiles compared to results obtained on P3 Mice myeloid cell line. FACs analysis of these antiproliferative effects on U2OS human osteosarcoma cell line exhibited cell cycle phase arrests at G1, G1/S or S. This suspects similar mechanism of cell division arrest in U2OS cell induced by these studied compounds to that induced by the apoptotic prodigiosin who differs to that induced by undecylprodigiosin, daunorubicin or other known anthracycline analogues. Thus, these red-like pigments without antibiotic effect unlike prodiginines and anthracyclines could constitute novel related compounds presenting a strong potential for their contribution in anticancer chemotherapy.

Keywords:
pigment anthracycline antiproliferative cancer cells cycle phase arrest S. coelicoflavus

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References:

[1]	Soliev A B, Hosokawa K and Enomoto K, Bioactive Pigments from Marine Bacteria: Applications and Physiological Roles, Evidence-Based Complementary and Alternative Medicine, eCAM, 2011, 670349.
[2]	Conn H J, Conn J E, Value of Pigmentation in Classifying Actinomycetes: A Preliminary Note. J Bacteriol, 42 (6). 791-799. Dec 1941.
[3]	Ayoubi H, Mouslim A, Moujabbir S, Amine S, Azougar I, Mouslim J and Menggad M, Isolation and phenotypic characterization of actinomycetes from Rabat neighborhood soil and their potential to produce bioactive compounds, Afr J Microbiol Res, 12 (8). 186-191. Feb 2018.
[4]	Nadas J and Sun D Anthracyclines as effective anticancer drugs. Expert Opin Drug Discov, 1 (6). 549-68. Nov 2006.
[5]	Zhang Z, Gong YK, Zhou Q, Hu Y, Ma HM, Chen YS, Igarashi Y, Pan L and Tang GL, Hydroxyl regioisomerization of anthracycline catalyzed by a four-enzyme cascade, Proc Natl Acad Sci, 114 (7). 1554-1559. Feb 2017.
[6]	Das A and Khosla C, Biosynthesis of aromatic polyketides in bacteria, Acc Chem Res, 42 (5). 631-9. Mar 2009.
[7]	Khosla C, Gokhale R S, Jacobsen J R and Cane D E, Tolerance and specificity of polyketide synthases, Annu Rev Biochem, 68. 219-253. Jul 1999.
[8]	Bartel PL, Connors NC and Strohl WR, Biosynthesis of anthracyclines: analysis of mutants of Streptomyces sp. strain C5 blocked in daunomycin biosynthesis, J Gen Microbiol, 136. 1877-1886. Jun 1990.
[9]	Connors NC, Bartel PL and Strohl WR, Biosynthesis of anthracyclines: enzymatic conversion of aklanonic acid to aklavinone and ε-rhodomycinone by anthracycline-producing streptomycetes, J Gen Microbiol, 136. 1887-1894. May1990.
[10]	Eckardt K and Wagner C, Biosynthesis of anthracyclinones, J Basic Microbiol, 28 (1-2). 137-144. 1988.
[11]	Coombs C C, Tavakkoli M and Tallman M S, Acute promyelocytic leukemia: where did we start, where are we now, and the future, Blood Cancer Journal, 2015 Apr 17, 5(4): e304.
[12]	Arcamone F, Antitumor anthracyclines: recent developments. Med Res Rev, 4 (2). 153-188. Apr-Jun 1984.
[13]	Grein A, Spalla C, di Marco A, and Canevazzi G, “Descrizione e classificazione di un attinomicete (Streptomyces peucetius sp. nova). Produttore di una sostanza ad attivit antitumorale: la daunomicina”, Giorn Microbiol, 11. 109-118. (Italian). (1963).
[14]	Minotti G, Menna P, Salvatorelli E, Cairo G and Gianni L, Anthracyclines: Molecular Advances and Pharmacologic Developments in Antitumor Activity and Cardiotoxicity, Pharmacol Rev, 56 (2). 185-229. Jun 2004.
[15]	Dartsch DC, Schaefer A, Boldt S, Kolch W and Marquardt H, Comparison of anthracycline-induced death of human leukemia cells: Programmed cell death versus necrosis, Apoptosis, 7 (6). 537-548. Dec 2002.
[16]	Ferraro C, Quemeneur L, Prigent AF, Taverne C, Revillard JP, et al. Anthracyclines trigger apoptosis of both G0-G1 and cycling peripheral blood lymphocytes and induce massive deletion of mature T and B cells, Cancer Res, 60 (7). 1901-1907. Dec 2000.
[17]	Mort MK, Sen JM, Morris AL, DeGregory KA, McLoughlin EM, Mort JF, Dunn SP, Abuannadi M and Keng MK, Evaluation of cardiomyopathy in acute myeloid leukemia patients treated with anthracyclines, J Oncol Pharm Pract, 2019 Sep 9: 1078155219873014.
[18]	Khan MA, D'Ovidio A, Tran H and Palaniyar N, Anthracyclines Suppress Both NADPH Oxidase-Dependent and -Independent NETosis in Human Neutrophils, Cancers, 2019, 11 (9).
[19]	Wang AHJ, Intercalative drug binding to DNA, Curr Opin Struct Biol, 2 (3). 361-368. Jun 1992.
[20]	Gewirtz DA, A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin, Biochem Pharmacol, 57 (7). 727-741. Apr 1999.
[21]	Guano F, Pourquier P, Tinelli S, Binaschi M, Bigioni M, Animati F, Manzini S, Zunino F, Kohlhagen G, Pommier Y and Capranico G. Topoisomerase poisoning activity of novel disaccharide anthracyclines, Mol Pharmacol, 56 (1). 77-84. Jul 1999.
[22]	Bertheau P, Plassa F, Espie M, Turpin E, de Roquancourt A, Marty M, Lerebours F, Beuzard Y, Janin A, and de The H, Effect of mutated TP53 on response of advanced breast cancers to high-dose chemotherapy, Lancet, 360 (9336). 852-854. Sep 2002.
[23]	Kiyomiya K, Matsuo S, and Kurebe M, Mechanism of specific nuclear transport of adriamycin: the mode of nuclear translocation of adriamycin-proteasome complex, Cancer Res, 61 (6). 2467-2471. Apr 2001.
[24]	Plastaras JP, Dedon PC, and Marnett LJ, Effects of DNA structure on oxopropenylation by the endogenous mutagens malondialdehyde and base propenal, Biochemistry, 41 (16). 5033-5042. Apr 2002.
[25]	Bigioni M, Salvatore C, Bullo A, Bellarosa D, Iafrate E, Animati F, Capranico G, Goso C, Maggi CA, Pratesi G, et al, A comparative study of cellular and molecular pharmacology of doxorubicin and MEN 10755, a disaccharide analogue, Biochem Pharmacol, 62 (1): 63-70. Jul 2001.
[26]	Ling Y H, el-Naggar A K, Priebe W and Perez-Soler R, Cell cycle-dependent cytotoxicity, G2/M phase arrest, and disruption of p34cdc2/cyclin B1 activity induced by doxorubicin in synchronized P388 cells, Molecular Pharmacology, 49 (5). 832-841. May 1996.
[27]	Elmore LW, Rehder CW, Di X, McChesney PA, Jackson-Cook CK, Gewirtz DA and Holt SE, Adriamycin-induced senescence in breast tumor cells involves functional p53 and telomere dysfunction; J Biol Chem, 277 (38): 35509-35515. Oct 2002.
[28]	Zhang W, Kornblau SM, Kobayashi T, Gambel A, Claxton D and Deisseroth AB, High levels of constitutive WAF1/Cip1 protein are associated with chemoresistance in acute myelogenous leukemia, Clin Cancer Res, 1 (9). 1051-1057. Sep 1995.
[29]	Lüpertz R, Wätjen W, Kahl R and Chovolou Y, Dose- and time-dependent effects of doxorubicin on cytotoxicity, cell cycle and apoptotic cell death in human colon cancer cells, Toxicology, 271 (3). 115-21. May 2010.
[30]	Chang CC, Chen WC, Ho SF, Wu HS and Wei YH, Development of natural anti-tumor drugs by microorganisms, J Biosci Bioeng, 111 (5). 501-511. May 2011.
[31]	Williamson NR, Fineran PC, Gristwood T, Chawrai SR, Leeper FJ, Salmond GPC Anticancer and immunosuppressive properties of bacterial prodiginines, Future Microbiol, 2 (6). 605-618. Dec 2007.
[32]	Vogelstein B, Lane D and Levine AJ, Surfing the p53 network, Nature, 408 (6810). 307-10. Nov 2000.
[33]	Perez-Tomas R and Montaner B. Effects of the proapoptotic drug prodigiosin on cell cycle-related proteins in Jurkat T cells. Histol Histopathol. 18 (2003): 379-85.
[34]	Liu P, Wang Y, Qi X, Gu Q, Geng M, Li J. Undecylprodigiosin Induced Apoptosis in P388 Cancer Cells Is Associated with Its Binding to Ribosome. St-Pierre Y, ed. PLoS ONE. 8 (2013): e65381.
[35]	Dalili D, Fouladdel Sh, Rastkari N, Samadi N, Ahmadkhaniha R, Ardavan A and Azizi E, Prodigiosin, the red pigment of Serratia marcescens, shows cytotoxic effects and apoptosis induction in HT-29 and T47D cancer cell lines, Natural Product Research, 26 (22). 2078-2083. 2012.
[36]	Mortellaro A, Songia S, Gnocchi P, Ferrari M, Fornasiero C, D'Alessio R, Isetta A, Colotta F and Golay J, New immunosuppressive drug PNU156804 blocks IL-2-dependent proliferation and NF-kappa B and AP-1 activation, J Immunol, 162 (12). 7102-7109. Jul 1999.
[37]	Songia S, Mortellaro A, Taverna S, Fornasiero C, Scheiber EA, Erba E, Colotta F, Mantovani A, Isetta AM, Golay J, Characterization of the new immunosuppressive drug undecylprodigiosin in human lymphocytes: retinoblastoma protein, cyclin-dependent kinase-2, and cyclin-dependent kinase-4 as molecular targets, J Immunol, 158 (8). 3987-95. Apr 1997.
[38]	Myers C E, Mimnaugh E G, Yeh G C and Sinha B K, Biochemical mechanisms of tumor cell kill by anthracyclines. In Antbraycline and Anthracenedione-Based Anti-Cancer Agents, pp. 527-569. Edited by J. W. Lown. Amsterdam: Elsevier. (1988).
[39]	Mouslim A, Ayoubi H, Moujabbir S, Mouslim J and Menggad M, Physico-chemical Characterization of a Pink Red-like Pigments Produced by Five New Bacterial Soil Strains Identified as Streptomyces coelicoflavus, Am J Microbiol Res, 6 (3). 67-72. Jun 2018.
[40]	Holkar S, Begde D, Nashikkar N, Kadam T and Upadhyay A, Rhodomycin analogues from Streptomyces purpurascens: isolation, characterization and biological activities, SpringerPlus, 2(1). 93. (13p). Mar 2013.
[41]	Rudd BA and Hopwood DA, A Pigmented Mycelial Antibiotic in Streptomyces coelicolor: Control by a Chromosomal Gene Cluster. Journal of General Microbiology, 119 (2). 333-340. Aug 1980.
[42]	Williams RP, Green JA and Rappoport DA, Studies on pigmentation of Serratia marcescens. I. spectral and paper chromatographic properties of Prodigiosin, J Bacteriol, 71 (1). 115-120. Jan 1956.
[43]	Elahian F, Moghimi B, Dinmohammadi F, Ghamghami M, Hamidi M and Mirzaei S A, The Anticancer Agent Prodigiosin Is Not a Multidrug Resistance Protein Substrate, DNA and Cell Biology, 32 (3). 90-97. Mar 2013.
[44]	Faheem AR, Anthracyclines: Mechanism of Action, Classification, Pharmacokinetics and Future - A Mini Review, Int J Biotech & Bioeng, 4 (4). 81-85. Apr 2018.
[45]	Bonvini P, Zorzi E, Basso G and Rosolen A, Bortezomib-mediated 26S proteasome inhibition causes cell-cycle arrest and induces apoptosis in CD-30 þ anaplastic large cell lymphoma, Leukemia, 21 (4). 838-842. Apr 2007.