Skip to main content

Advertisement

Log in

A Non-digestible Fraction of the Common Bean (Phaseolus vulgaris L.) Induces Cell Cycle Arrest and Apoptosis During Early Carcinogenesis

  • Original Paper
  • Published:
Plant Foods for Human Nutrition Aims and scope Submit manuscript

Abstract

We have previously demonstrated that the non-digestible fraction (NDF) from common cooked beans (P. vulgaris L., cv Negro 8025) inhibits azoxymethane (AOM)-induced colon cancer and influences the expression of genes involved in the induction of apoptosis and cell cycle arrest through the action of butyrate. The objective of this study was to identify cell cycle alterations and morphological changes induced by treatment with AOM and to examine the formation of colonic aberrant crypt foci (ACF) in male Sprague Dawley rats fed with these beans. Rats were fed control diets upon arrival and were randomly placed into four groups after one week of acclimatization: control, NDF (intragastric administration), NDF + AOM and AOM. Rats treated with NDF + AOM exhibited a significantly lower number of total colonic ACF with a notable increase in the number of cells present in the G1 phase (83.14 %); a decreased proliferation index was observed in the NDF + AOM group when compared to AOM group. NDF + AOM also displayed a higher number of apoptotic cells compared to AOM group. NDF of cooked common beans inhibited colon carcinogenesis at an early stage by inducing cell cycle arrest of colon cells and morphological changes linked to apoptosis, thus confirming previous results obtained with gene expression studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

CRC:

Colorectal cancer

SCFAs:

Short-chain fatty acids

AOM:

Azoxymethane

ACF:

Aberrant crypt foci

NDF:

Non-digestible fraction

H&E:

Hematoxylin and eosin

TUNEL:

Terminal deoxynucleotidyl transferase nick end-labeling

ANOVA:

One way variance analysis

PE:

Polysaccharide extract

B. lactis :

Bifidobacterium lactis

G1 :

Growth 1 (cell cycle)

S:

Synthesis (cell cycle)

G2 :

Growth 2 (cell cycle)

M:

Mitosis (cell cycle)

G0 :

Resting (cell cycle)

References

  1. Instituto Nacional de Estadística, Geografía e Informática. INEGI. 2008 www.inegi.gob.mx

  2. Paredes-López O, Guzmán-Maldonado H, Serna-Saldívar S (2000) Los alimentos mágicos de las culturas indígenas de México- El caso de la tortilla; El Colegio de Sinaloa City: Culiacán. Sinaloa, México

    Google Scholar 

  3. Campos-Vega R, Oomah BD, Vergara-Castañeda HA (2012) Chapter: Functional compounds sources: Beans in sight. In: E. Popescu and Iv. Golubev (Eds) Beans: Nutrition, Consumption and Health 1st edn. Nova Science Publishers, Inc

  4. Feregrino-Pérez AA, Berumen LC, García-Alcocer G, Guevara-Gónzalez R, Ramos-Gomez M, Reynoso-Camacho R, Acosta-Gallegos JA, Loarca-Piña G (2008) Composition and chemopreventive effect of polysaccharides from common beans (Phaseolus vulgaris L.) on azoxymethane-induced colon cancer. J Agric Food Chem 56:8737–8744

    Article  Google Scholar 

  5. Aparicio-Fernández X, Manzo-Bonilla L, Loarca-Piña GF (2005) Comparison of antimutagenic activity of phenolic compounds in newly harvested and stored common beans Phaseolus vulgaris against aflatoxin B1. J Food Sci 70:S73–S78

    Article  Google Scholar 

  6. Kurtzman RHJR, Halbrook WU (1970) Polysaccharides from dry navy beans, Phaseolus vulgaris: its isolation and stimulation of Clostridium perfringens. Appl Microbiol 20(5):715–719

    CAS  Google Scholar 

  7. Association of Oficial Analytical Chemists. Official Methods of Analysis. (2002) 17th ed. AOAC, Arlington, VA. Methods 920.105, 925.23, 945.46, 985.29 and 991.43; 70:807–811

  8. Bird RP (1987) Observation and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: preliminary findings. Cancer Lett 30:147–151

    Article  Google Scholar 

  9. Hedley DW, Friedlander ML, Taylor IW, Rugg CA, Musgrone EA (1983) Method for analysis of cellular DNA content of paraffin-embedded pathological material using flow cytometry. J Histochem Cytochem 31(11):1333–1335

    Article  CAS  Google Scholar 

  10. Vergara-Castañeda HA, Guevara-González RG, Ramos-Gómez M, Reynoso-Camacho R, Guzmán-Maldonado H, Feregrino-Pérez AA, Oomah BD, Loarca-Piña G (2010) Non-digestible fraction of cooked bean (Phaseolus vulgaris L.) cultivar bayo madero suppresses colonic aberrant crypt foci in azoxymethane-induced rats. Food Funct 1(3):294–300. doi:10.1039/C0FO00130A

    Article  Google Scholar 

  11. Costa de Oliveira A, Silva Queiroz K, Machado S, Carraro F (2001) O processamento domestico do feijao-comun ocasionau uma reducao nos fatores antinutricionais fitato e taninos, no teor de amido e em fatores de flatulencia rafinose, estaquiose e verbascose. Arch Latinoam Nutr 51:276–283, ISSN 0004–0622

    Google Scholar 

  12. Cruz-Bravo RK, Guevara-Gonzalez R, Ramos-Gomez M, Garcia-Gasca T, Campos-Vega R, Oomah BD, Loarca-Piña G (2011) Fermented nondigestible fraction from common bean (Phaseolus vulgaris L.) cultivar negro 8025 modulates HT-29 cell behavior. J Food Sci 76(2):T41–T47. doi:10.1111/j.1750-3841.2010.02025.x

    Article  CAS  Google Scholar 

  13. Le Leu RK, Hu Y, Brown IL, Woodman RJ, Young GP (2010) Synbiotic intervention of Bifidobacterium lactis and resistant starch protects against colorectal cancer development in rats. Carcinogenesis 31(2):246–251. doi:10.1093/carcin/bgp197

    Article  Google Scholar 

  14. Nakanishi S, Kataoka K, Kuwahara T, Ohnishi Y (2003) Effects of high amylose maize starch and Clostridium butyricum on metabolism in colonic microbiota and formation of azoxymethane induced aberrant crypt foci in the rat colon. Microbiol Immunol 47(12):951–958

    Article  CAS  Google Scholar 

  15. Hernández-Salazar M, Guevara-González RG, Cruz-Hernández A, Guevara-Olvera L, Bello-Pérez LA, Castaño-Tostado E, Loarca-Piña G (2013) Flaxseed (Linum usitatissimum L.) and its total non-digestible fraction influence the expression of genes involved in azoxymethane-induced colon cancer in rats. Plant Foods Hum Nutr 68(3):259–267

  16. Busambwa K, Miller-Cebert RL, Aboagye L, Dalrymple L, Boateng J, Shackelford L, Walker LT, Verghese M (2014) Inhibitory effect of lentils, green split and yellow peas (sprouted and non-sprouted) on azoxymethane-induced aberrant crypt foci in Fisher 344 male rats. Inter J Cancer Res 10(1):27–36

  17. Lahouar L, Pochart P, Salem HB, El Felah M, Mokni M, Magne F, Mangin I, Suau A, Pereira E, Hammami M, Achour L (2012) Effect of dietary fibre of barley variety “rihane” on azoxymethane-induced aberrant crypt foci development and on colonic microbiota diversity in rats. Br J Nutr 108(11):2034–2042

    Article  CAS  Google Scholar 

  18. Lazarova D, Lee A, Wong T, Marian B, Chiaro C, Rainey C, Bordonaro M (2014) Modulation of Wnt activity and cell physiology by butyrate in LT97 microadenoma cells. J Cancer Educ 5(3):203

    Article  CAS  Google Scholar 

  19. Lee EJ, Sung MK (2003) Chemoprevention of azoxymethane-induced rat colon carcinogenesis by seatangle, a fiber-rich seaweed. Plant Foods Hum Nutr 58(3):1–8

    Article  Google Scholar 

  20. Campos-Vega R, Oomah BD, Loarca-Piña G, Vergara-Castañeda HA (2013) Common beans and their non-digestible fraction: cancer inhibitory activity—an overview. Foods 2(3):374–392

    Article  Google Scholar 

  21. Mendoza-Díaz S, Ortiz-Valerio M del C, Castaño-Tostado E, Figueroa-Cárdenas J de D, Reynoso-Camacho R, Ramos-Gómez M, Campos-Vega R, Loarca-Piña G (2012) Antioxidant capacity and antimutagenic activity of anthocyanin and carotenoid extracts from nixtamalized pigmented creole maize races (Zea mays L.). Plant Foods Hum Nutr 67(4):442–449

  22. Thompson CB (1995) Apoptosis in the pathogenesis and treatment of disease. Sci 267(5203):1456–1462

    Article  CAS  Google Scholar 

  23. Hu Y, Martin J, Le Leu R, Young GP (2002) The colonic response to genotoxic carcinogens in the rats: regulation by dietary fibre. Carcinogenesis 23(7):1131–1137

    Article  CAS  Google Scholar 

  24. Le Leu RK, Brown IL, Hu Y, Bird AR, Jackson M, Esterman A, Young GP (2005) A synbiotic combination of resistant starch and Bifidobacterium lactis facilitates apoptotic deletion of carcinogen-damaged cells in rat colon. J Nutr 135:996–1001

    Google Scholar 

  25. Utama Z, Okazaki Y, Tomotake H, Kato N (2013) Tempe consumption modulates fecal secondary bile acids, mucins, immunoglobulin a, enzyme activities, and cecal microflora and organic acids in rats. Plant Foods Hum Nutr 68(2):177–183

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Consejo Nacional de Ciencia y Tecnología (CONACYT) grant No. 57536 and the Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias (INIFAP, Celaya).

Conflicts of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guadalupe Loarca-Piña.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Feregrino-Perez, A.A., Piñol-Felis, C., Gomez-Arbones, X. et al. A Non-digestible Fraction of the Common Bean (Phaseolus vulgaris L.) Induces Cell Cycle Arrest and Apoptosis During Early Carcinogenesis. Plant Foods Hum Nutr 69, 248–254 (2014). https://doi.org/10.1007/s11130-014-0428-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11130-014-0428-7

Keywords

Navigation