Discovery of an antitumor compound from xenorhabdus stockiae HN_xs01.

Antitumor Apoptosis Secondary metabolite Xenorhabdus

Journal

World journal of microbiology & biotechnology
ISSN: 1573-0972
Titre abrégé: World J Microbiol Biotechnol
Pays: Germany
ID NLM: 9012472

Informations de publication

Date de publication:
17 Feb 2024
Historique:
received: 25 04 2023
accepted: 01 02 2024
medline: 17 2 2024
pubmed: 17 2 2024
entrez: 17 2 2024
Statut: epublish

Résumé

Xenorhabdus, known for its symbiotic relationship with Entomopathogenic nematodes (EPNs), belongs to the Enterobacteriaceae family. This dual-host symbiotic nematode exhibits pathogenic traits, rendering it a promising biocontrol agent against insects. Our prior investigations revealed that Xenorhabdus stockiae HN_xs01, isolated in our laboratory, demonstrates exceptional potential in halting bacterial growth and displaying anti-tumor activity. Subsequently, we separated and purified the supernatant of the HN_xs01 strain and obtained a new compound with significant inhibitory activity on tumor cells, which we named XNAE. Through LC-MS analysis, the mass-to-nucleus ratio of XNAE was determined to be 254.24. Our findings indicated that XNAE exerts a time- and dose-dependent inhibition on B16 and HeLa cells. After 24 h, its IC

Identifiants

pubmed: 38366186
doi: 10.1007/s11274-024-03915-1
pii: 10.1007/s11274-024-03915-1
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

101

Subventions

Organisme : National Natural Science Foundation of China
ID : 32070090
Organisme : Research Foundation of Education Bureau of Hunan Province
ID : 19K053

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Amaning Danquah C, Minkah PAB, Osei Duah Junior I, Amankwah KB, Somuah SO (2022) Antimicrobial compounds from microorganisms. Antibiotics 11:285. https://doi.org/10.3390/antibiotics11030285
doi: 10.3390/antibiotics11030285 pubmed: 35326749 pmcid: 8944786
Arrigo KR (2004) Marine microorganisms and global nutrient cycles. Nature 437:349–355. https://doi.org/10.1038/nature04159
doi: 10.1038/nature04159
Awori RM (2022) Nematophilic bacteria associated with entomopathogenic nematodes and drug development of their biomolecules. Front Microbiol 13:993688. https://doi.org/10.3389/fmicb.2022.993688
doi: 10.3389/fmicb.2022.993688 pubmed: 36187939 pmcid: 9520725
Bertrand S, Bohni N, Schnee S, Schumpp O, Gindro K, Wolfender JL (2014) Metabolite induction via microorganism co-culture: a potential way to enhance chemical diversity for drug discovery. Biotechnol Adv 32:1180–1204. https://doi.org/10.1016/j.biotechadv.2014.03.001
doi: 10.1016/j.biotechadv.2014.03.001 pubmed: 24651031
Booysen E, Dicks LMT (2020) Does the Future of Antibiotics Lie in secondary metabolites produced by Xenorhabdus spp.? A review. Probiotics Antimicrob Proteins 12:1310–1320. https://doi.org/10.1007/s12602-020-09688-x
doi: 10.1007/s12602-020-09688-x pubmed: 32844362
Challinor VL, Bode HB (2015) Bioactive natural products from novel microbial sources. Ann N Y Acad Sci 1354:82–97. https://doi.org/10.1111/nyas.12954
doi: 10.1111/nyas.12954 pubmed: 26509922
Chen G, Zhu N, Tang Z, Ye P, Hu Z, Liu L (2013) Resource availability shapes microbial motility and mediates early-stage formation of microbial clusters in biological wastewater treatment processes. Appl Microbiol Biotechnol 98:1459–1467. https://doi.org/10.1007/s00253-013-5109-1
doi: 10.1007/s00253-013-5109-1 pubmed: 23907257
Cimen H, Touray M, Gulsen SH, Hazir S (2022) Natural products from Photorhabdus and Xenorhabdus: mechanisms and impacts. Appl Microbiol Biotechnol 106:4387–4399. https://doi.org/10.1007/s00253-022-12023-9
doi: 10.1007/s00253-022-12023-9 pubmed: 35723692
Crawford JM, Kontnik R, Clardy J (2010) Regulating alternative lifestyles in Entomopathogenic Bacteria. Curr Biol 20:69–74. https://doi.org/10.1016/j.cub.2009.10.059
doi: 10.1016/j.cub.2009.10.059 pubmed: 20022247 pmcid: 2821981
Dreyer J, Malan AP, Dicks LMT (2018) Bacteria of the Genus Xenorhabdus, a Novel source of Bioactive compounds. Front Microbiol 9:3177. https://doi.org/10.3389/fmicb.2018.03177
doi: 10.3389/fmicb.2018.03177 pubmed: 30619229 pmcid: 6305712
Dreyer J, Rautenbach M, Booysen E, van Staden AD, Deane SM, Dicks LMT (2019) Xenorhabdus Khoisanae SB10 produces Lys-rich PAX lipopeptides and a xenocoumacin in its antimicrobial complex. BMC Microbiol 19:132. https://doi.org/10.1186/s12866-019-1503-x
doi: 10.1186/s12866-019-1503-x pubmed: 31195965 pmcid: 6567599
Goodrich-Blair H, Clarke DJ (2007) Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Mol Microbiol 64:260–268. https://doi.org/10.1111/j.1365-2958.2007.05671.x
doi: 10.1111/j.1365-2958.2007.05671.x pubmed: 17493120
Guilpain P, Mouthon L (2008) Antiendothelial cells autoantibodies in Vasculitis-Associated systemic diseases. Clin Rev Allergy Immunol 35:59–65. https://doi.org/10.1007/s12016-007-8069-3
doi: 10.1007/s12016-007-8069-3 pubmed: 18228162
Hida K, Maishi N, Torii C, Hida Y (2016) Tumor angiogenesis—characteristics of tumor endothelial cells. Int J Clin Oncol 21:206–212. https://doi.org/10.1007/s10147-016-0957-1
doi: 10.1007/s10147-016-0957-1 pubmed: 26879652
Horbay R, Bilyy R (2016) Mitochondrial dynamics during cell cycling. Apoptosis 21:1327–1335. https://doi.org/10.1007/s10495-016-1295-5
doi: 10.1007/s10495-016-1295-5 pubmed: 27658785
Hu S, Fu J, Huang F, Ding X, Stewart AF, Xia L, Zhang Y (2014) Genome engineering of Agrobacterium tumefaciens using the lambda red recombination system. Appl Microbiol Biotechnol 98:2165–2172. https://doi.org/10.1007/s00253-013-5412-x
doi: 10.1007/s00253-013-5412-x pubmed: 24297480
Huang X, Sun Y, Liu S, Li Y, Li C, Sun Y, Ding X, Xia L, Hu Y, Hu S (2022) Recombineering using RecET-like recombinases from Xenorhabdus and its application in mining of natural products. Appl Microbiol Biotechnol 106:7857–7866. https://doi.org/10.1007/s00253-022-12258-6
doi: 10.1007/s00253-022-12258-6 pubmed: 36326838
Jensen PR, Moore BS, Fenical W (2015) The marine actinomycete genus Salinispora: a model organism for secondary metabolite discovery. Nat Prod Rep 32:738–751. https://doi.org/10.1039/c4np00167b
doi: 10.1039/c4np00167b pubmed: 25730728 pmcid: 4414829
Justus CR, Marie MA, Sanderlin EJ, Yang LV (2023) Transwell in Vitro Cell Migration and Invasion assays. 2644 349–359. https://doi.org/10.1007/978-1-0716-3052-5_22
Ma J, Gu Y, Xu P (2020) A roadmap to engineering antiviral natural products synthesis in microbes. Curr Opin Biotechnol 66:140–149. https://doi.org/10.1016/j.copbio.2020.07.008
doi: 10.1016/j.copbio.2020.07.008 pubmed: 32795662 pmcid: 7419324
Manfredi JJ (2003) p53 and apoptosis: it’s not just in the nucleus anymore. Mol Cell 11:552–554. https://doi.org/10.1016/s1097-2765(03)00106-0
doi: 10.1016/s1097-2765(03)00106-0 pubmed: 12667439
Mastore M, Caramella S, Quadroni S, Brivio MF (2021) Drosophila Suzukii susceptibility to the oral administration of Bacillus thuringiensis, Xenorhabdus nematophila and its secondary metabolites. Insects 12. https://doi.org/10.3390/insects12070635
Medison RG, Tan L, Medison MB, Chiwina KE (2022) Use of beneficial bacterial endophytes: a practical strategy to achieve sustainable agriculture. AIMS Microbiol 8:624–643. https://doi.org/10.3934/microbiol.2022040
doi: 10.3934/microbiol.2022040 pubmed: 36694581 pmcid: 9834078
Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, Moll UM (2003) p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11:577–590. https://doi.org/10.1016/s1097-2765(03)00050-9
doi: 10.1016/s1097-2765(03)00050-9 pubmed: 12667443
Mollah MMI, Kim Y (2020) Virulent secondary metabolites of entomopathogenic bacteria genera, Xenorhabdus and Photorhabdus, inhibit phospholipase A(2) to suppress host insect immunity. BMC Microbiol 20:359. https://doi.org/10.1186/s12866-020-02042-9
doi: 10.1186/s12866-020-02042-9 pubmed: 33228536 pmcid: 7684946
Murillo J, Thanwisai A, Tandhavanant S, Saiprom N, Waterfield NR, Ke Long P, Bode HB, Peacock SJ, Chantratita N (2012) Diversity of Xenorhabdus and Photorhabdus spp. and their Symbiotic Entomopathogenic nematodes from Thailand. PLoS ONE 7:e43835. https://doi.org/10.1371/journal.pone.0043835
doi: 10.1371/journal.pone.0043835
Naito H, Wakabayashi T, Kidoya H, Muramatsu F, Takara K, Eino D, Yamane K, Iba T, Takakura N (2016) Endothelial side Population cells contribute to Tumor Angiogenesis and Antiangiogenic Drug Resistance. Cancer Res 76:3200–3210. https://doi.org/10.1158/0008-5472.can-15-2998
doi: 10.1158/0008-5472.can-15-2998 pubmed: 27197162
Pacciani-Mori L, Suweis S, Maritan A, Giometto A (2021) Constrained proteome allocation affects coexistence in models of competitive microbial communities. ISME J 15:1458–1477. https://doi.org/10.1038/s41396-020-00863-0
doi: 10.1038/s41396-020-00863-0 pubmed: 33432139 pmcid: 8115080
Pantel L, Florin T, Dobosz-Bartoszek M, Racine E, Sarciaux M, Serri M, Houard J, Campagne JM, de Figueiredo RM, Midrier C, Gaudriault S, Givaudan A, Lanois A, Forst S, Aumelas A, Cotteaux-Lautard C, Bolla JM, Vingsbo Lundberg C, Huseby DL, Hughes D, Villain-Guillot P, Mankin AS, Polikanov YS, Gualtieri M (2018) Odilorhabdins, Antibacterial Agents that Cause Miscoding by Binding at a New Ribosomal Site. Molecular cell 70: 83–94 e https://doi.org/10.1016/j.molcel.2018.03.001
Prabha S, Sharma B, Labhasetwar V (2012) Inhibition of tumor angiogenesis and growth by nanoparticle-mediated p53 gene therapy in mice. Cancer Gene Ther 19:530–537. https://doi.org/10.1038/cgt.2012.26
doi: 10.1038/cgt.2012.26 pubmed: 22595792 pmcid: 3400709
Primiceri E, Chiriacò MS, Dioguardi F, Monteduro AG, D’Amone E, Rinaldi R, Giannelli G, Maruccio G (2011) Automatic transwell assay by an EIS cell chip to monitor cell migration. Lab Chip 11:4081. https://doi.org/10.1039/c1lc20540d
doi: 10.1039/c1lc20540d pubmed: 22012570
Racine E, Gualtieri M (2019) From worms to drug candidate: the Story of odilorhabdins, a New Class of Antimicrobial agents. Front Microbiol 10:2893. https://doi.org/10.3389/fmicb.2019.02893
doi: 10.3389/fmicb.2019.02893 pubmed: 31921069 pmcid: 6930155
Ruiz-Losada M, Gonzalez R, Peropadre A, Gil-Galvez A, Tena JJ, Baonza A, Estella C (2022) Coordination between cell proliferation and apoptosis after DNA damage in Drosophila. Cell Death Differ 29:832–845. https://doi.org/10.1038/s41418-021-00898-6
doi: 10.1038/s41418-021-00898-6 pubmed: 34824391
Sahai E (2007) Illuminating the metastatic process. Nat Rev Cancer 7:737–749. https://doi.org/10.1038/nrc2229
doi: 10.1038/nrc2229 pubmed: 17891189
Salazar-Roa M, Malumbres M (2017) Fueling the Cell Division Cycle. Trends Cell Biol 27:69–81. https://doi.org/10.1016/j.tcb.2016.08.009
doi: 10.1016/j.tcb.2016.08.009 pubmed: 27746095
Schrenk MO, Huber JA, Edwards KJ (2010) Microbial provinces in the Subseafloor. Annual Rev Mar Sci 2:279–304. https://doi.org/10.1146/annurev-marine-120308-081000
doi: 10.1146/annurev-marine-120308-081000
Shi YM, Bode HB (2018) Chemical language and warfare of bacterial natural products in bacteria-nematode-insect interactions. Nat Prod Rep 35:309–335. https://doi.org/10.1039/c7np00054e
doi: 10.1039/c7np00054e pubmed: 29359226
Shi YM, Hirschmann M, Shi YN, Ahmed S, Abebew D, Tobias NJ, Grun P, Crames JJ, Poschel L, Kuttenlochner W, Richter C, Herrmann J, Muller R, Thanwisai A, Pidot SJ, Stinear TP, Groll M, Kim Y, Bode HB (2022) Global analysis of biosynthetic gene clusters reveals conserved and unique natural products in entomopathogenic nematode-symbiotic bacteria. Nat Chem. https://doi.org/10.1038/s41557-022-00923-2
doi: 10.1038/s41557-022-00923-2 pubmed: 36329179 pmcid: 9177418
Singh S, Orr D, Divinagracia E, McGraw J, Dorff K, Forst S (2015) Role of secondary metabolites in establishment of the mutualistic partnership between Xenorhabdus nematophila and the entomopathogenic nematode Steinernema carpocapsae. Appl Environ Microbiol 81:754–764. https://doi.org/10.1128/AEM.02650-14
doi: 10.1128/AEM.02650-14 pubmed: 25398871 pmcid: 4277586
Stoellinger HM, Alexanian AR (2022) Modifications to the Transwell Migration/Invasion Assay Method that eases assay performance and improves the Accuracy. Assay Drug Dev Technol 20:75–82. https://doi.org/10.1089/adt.2021.140
doi: 10.1089/adt.2021.140 pubmed: 35196113 pmcid: 8968842
Tietze A, Shi YN, Kronenwerth M, Bode HB (2020) Nonribosomal peptides produced by Minimal and Engineered synthetases with terminal reductase domains. Chembiochem: Eur J Chem Biology 21:2750–2754. https://doi.org/10.1002/cbic.202000176
doi: 10.1002/cbic.202000176
Tobias NJ, Wolff H, Djahanschiri B, Grundmann F, Kronenwerth M, Shi YM, Simonyi S, Grun P, Shapiro-Ilan D, Pidot SJ, Stinear TP, Ebersberger I, Bode HB (2017) Natural product diversity associated with the nematode symbionts Photorhabdus and Xenorhabdus. Nat Microbiol 2:1676–1685. https://doi.org/10.1038/s41564-017-0039-9
doi: 10.1038/s41564-017-0039-9 pubmed: 28993611
Tobias NJ, Shi YM, Bode HB (2018) Refining the natural product repertoire in Entomopathogenic Bacteria. Trends Microbiol 26:833–840. https://doi.org/10.1016/j.tim.2018.04.007
doi: 10.1016/j.tim.2018.04.007 pubmed: 29801772
van der Meij A, Worsley SF, Hutchings MI, van Wezel GP (2017) Chemical ecology of antibiotic production by actinomycetes. FEMS Microbiol Rev 41:392–416. https://doi.org/10.1093/femsre/fux005
doi: 10.1093/femsre/fux005 pubmed: 28521336
Venkatesulu BP, Mahadevan LS, Aliru ML, Yang X, Bodd MH, Singh PK, Yusuf SW, Abe J-i, Krishnan S (2018) Radiation-Induced Endothelial Vascular Injury. JACC: Basic Translational Sci 3:563–572. https://doi.org/10.1016/j.jacbts.2018.01.014
doi: 10.1016/j.jacbts.2018.01.014
Wang Z, Cirino PC (2016) New and improved tools and methods for enhanced biosynthesis of natural products in microorganisms. Curr Opin Biotechnol 42:159–168. https://doi.org/10.1016/j.copbio.2016.05.003
doi: 10.1016/j.copbio.2016.05.003 pubmed: 27284635
Yamaguchp H, Ishii E, Tashiro K, Miyazaki S (2009) Role of umbilical vein endothelial cells in Hematopoiesis. Leuk Lymphoma 31:61–69. https://doi.org/10.3109/10428199809057585
doi: 10.3109/10428199809057585
Yang X, Hou X, Sun Y, Zhang G, Hu X, Xie Y, Mo X, Ding X, Xia L, Hu S (2019) Screening a fosmid library of Xenorhabdus stockiae HN_xs01 reveals SrfABC toxin that exhibits both cytotoxicity and injectable insecticidal activity. J Invertebr Pathol 167:107247. https://doi.org/10.1016/j.jip.2019.107247
doi: 10.1016/j.jip.2019.107247 pubmed: 31521727
Zaccone R, Caruso G (2019) Microbial enzymes in the Mediterranean Sea: relationship with climate changes. AIMS Microbiol 5:251–272. https://doi.org/10.3934/microbiol.2019.3.251
doi: 10.3934/microbiol.2019.3.251 pubmed: 31663060 pmcid: 6787352
Zhang S, Fang X, Tang Q, Ge J, Wang Y, Zhang X (2019a) CpxR negatively regulates the production of xenocoumacin 1, a dihydroisocoumarin derivative produced by Xenorhabdus nematophila. MicrobiologyOpen 8:e00674. https://doi.org/10.1002/mbo3.674
doi: 10.1002/mbo3.674 pubmed: 29888873
Zhang S, Liu Q, Han Y, Han J, Yan Z, Wang Y, Zhang X (2019b) Nematophin, an antimicrobial dipeptide compound from Xenorhabdus nematophila YL001 as a potent Biopesticide for Rhizoctonia Solani Control. Front Microbiol 10:1765. https://doi.org/10.3389/fmicb.2019.01765
doi: 10.3389/fmicb.2019.01765 pubmed: 31440217 pmcid: 6693444
Zhang D, Kaweme NM, Duan P, Dong Y, Yuan X (2021) Upfront treatment of Pediatric High-Risk Neuroblastoma with Chemotherapy, surgery, and Radiotherapy Combination: the CCCG-NB-2014 protocol. Front Oncol 11:745794. https://doi.org/10.3389/fonc.2021.745794
doi: 10.3389/fonc.2021.745794 pubmed: 34868944 pmcid: 8634583
Zhang C, Chen H, Huttel S, Hu S, Zhang W, Ding X, Yin J, Yin Y, Muller R, Xia L, Zhang Y, Tu Q (2022) A novel tumor-targeting strain of Xenorhabdus stockiae exhibits potent biological activities. Front Bioeng Biotechnol 10:984197. https://doi.org/10.3389/fbioe.2022.984197
doi: 10.3389/fbioe.2022.984197 pubmed: 36159678 pmcid: 9490112

Auteurs

Xiyin Huang (X)

State Key Laboratory of Developmental Biology of Freshwater Fish, Hunan Provincial Key Laboratory of Microbial Molecular Biology, College of Life Science, Hunan Normal University, No.36 Lushan Street, Changsha, 410081, China.

Qiong Tang (Q)

State Key Laboratory of Developmental Biology of Freshwater Fish, Hunan Provincial Key Laboratory of Microbial Molecular Biology, College of Life Science, Hunan Normal University, No.36 Lushan Street, Changsha, 410081, China.

Siqin Liu (S)

State Key Laboratory of Developmental Biology of Freshwater Fish, Hunan Provincial Key Laboratory of Microbial Molecular Biology, College of Life Science, Hunan Normal University, No.36 Lushan Street, Changsha, 410081, China.

Chen Li (C)

State Key Laboratory of Developmental Biology of Freshwater Fish, Hunan Provincial Key Laboratory of Microbial Molecular Biology, College of Life Science, Hunan Normal University, No.36 Lushan Street, Changsha, 410081, China.

Yaoguang Li (Y)

State Key Laboratory of Developmental Biology of Freshwater Fish, Hunan Provincial Key Laboratory of Microbial Molecular Biology, College of Life Science, Hunan Normal University, No.36 Lushan Street, Changsha, 410081, China.

Yunjun Sun (Y)

State Key Laboratory of Developmental Biology of Freshwater Fish, Hunan Provincial Key Laboratory of Microbial Molecular Biology, College of Life Science, Hunan Normal University, No.36 Lushan Street, Changsha, 410081, China.

Xuezhi Ding (X)

State Key Laboratory of Developmental Biology of Freshwater Fish, Hunan Provincial Key Laboratory of Microbial Molecular Biology, College of Life Science, Hunan Normal University, No.36 Lushan Street, Changsha, 410081, China.

Liqiu Xia (L)

State Key Laboratory of Developmental Biology of Freshwater Fish, Hunan Provincial Key Laboratory of Microbial Molecular Biology, College of Life Science, Hunan Normal University, No.36 Lushan Street, Changsha, 410081, China.

Shengbiao Hu (S)

State Key Laboratory of Developmental Biology of Freshwater Fish, Hunan Provincial Key Laboratory of Microbial Molecular Biology, College of Life Science, Hunan Normal University, No.36 Lushan Street, Changsha, 410081, China. shengbiaohu@hunnu.edu.cn.

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