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Low Micronutrient Intake May Accelerate the Degenerative Diseases of Aging Through Allocation of Scarce Micronutrients by Triage

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Low Micronutrient Intake May Accelerate the Degenerative Diseases of Aging Through Allocation of Scarce Micronutrients by Triage PERSPECTIVE Low micronutrient intake may accelerate the degenerative diseases of aging through allocation of scarce micronutrients by triage Bruce N. Ames* Nutrition and Metabolism Center, Children’s Hospital of Oakland Research Institute, 5700 Martin Luther King Jr. Way, Oakland, CA 94609 Contributed by Bruce N. Ames, October 6, 2006 (sent for review September 20, 2006) Inadequate dietary intakes of vitamins and minerals are widespread, most likely due to excessive consumption of energy-rich, micro- nutrient-poor, refined food. Inadequate intakes may result in chronic metabolic disruption, including mitochondrial decay. Deficien- cies in many micronutrients cause DNA damage, such as chromosome breaks, in cultured human cells or in vivo. Some of these defi- ciencies also cause mitochondrial decay with oxidant leakage and cellular aging and are associated with late onset diseases such as cancer. I propose DNA damage and late onset disease are consequences of a triage allocation response to micronutrient scarcity. Epi- sodic shortages of micronutrients were common during evolution. Natural selection favors short-term survival at the expense of long-term health. I hypothesize that short-term survival was achieved by allocating scarce micronutrients by triage, in part through an adjustment of the binding affinity of proteins for required micronutrients. If this hypothesis is correct, micronutrient deficiencies that trigger the triage response would accelerate cancer, aging, and neural decay but would leave critical metabolic functions, such as ATP production, intact. Evidence that micronutrient malnutrition increases late onset diseases, such as cancer, is discussed. A mul- tivitamin-mineral supplement is one low-cost way to ensure intake of the Recommended Dietary Allowance of micronutrients throughout life. oor nutrition has been linked to Table 1. Selected micronutrient inadequacy in the U.S. an increased risk of many dis- % ingesting less than eases, including cancer, heart Nutrient Population group the EAR from food disease, and diabetes. The hu- Pman diet requires both macronutrients, Minerals which are the main source of calories, Iron Women 14–50 years old 16 and micronutrients (Ϸ40 essential min- Magnesium All 56 erals, vitamins, and other biochemicals), Zinc All 12 which are required for virtually all met- Vitamins abolic and developmental processes. The B6 Women Ͼ71 years old 49 leading dietary sources of energy in the Folate Adult women 16 United States are abundant in carbohy- E All 93 drates and fats (1) but deficient in mi- C All 31 cronutrients (i.e., they are energy-dense Less than the EAR is used as a measure of inadequacy in populations (4, 5). The RDA is defined as 2 and nutrient-poor) (2). Such foods are standard deviations above the EAR. Data are from Moshfegh et al. (4). inexpensive and tasty and as a conse- quence are consumed excessively, partic- ularly by the poor (3). Thus, even in the folic acid intakes above the RDA ap- such as the brain with an accompanying United States (4), inadequate intake of pear to be necessary to minimize chro- loss of ambulatory activity (9, 13–16). some vitamins and minerals is common mosome breaks (10, 11). The importance of optimizing meta- (Table 1). Suboptimal consumption of bolic function to prevent mitochondrial micronutrients (4) often accompanies Micronutrient Deficiencies May decay is illustrated by feeding the mito- caloric excess (6, 88) and may be the Accelerate Mitochondrial Decay and chondrial metabolites acetyl carnitine norm among the obese and contribute Degenerative Diseases of Aging, (ALC) and lipoic acid (LA) to old rats. to the pathologies associated with obe- Such as Cancer Carnitine is used for transporting fatty sity. Mitochondrial decay appears to be a acids into the mitochondria; the main Significant chronic metabolic disrup- major contributor to aging and its asso- form of carnitine in the plasma is ALC. tion may occur when consumption of a ciated degenerative diseases, including LA is a mitochondrial coenzyme and is micronutrient is below the current Rec- cancer and neural decay (12). Mitochon- ommended Dietary Allowance (RDA) dria from old rats compared with those (7–10) but above the level that causes from young rats generate increased Author contributions: B.N.A. wrote the paper. acute symptoms. When one component amounts of oxidant by-products (13) and Conflict of interest statement: B.N.A. is a founder of Ju- venon, a company that has licensed the University of Cali- of the metabolic network is inadequate, have decreased membrane potential, fornia patent (B.N.A. and T. Hagen, inventors) on acetyl there may be a variety of repercussions respiratory control ratio, cellular oxygen carnitine plus lipoic acid for rejuvenating old mitochondria. in metabolism, including acceleration of consumption, and cardiolipin (a key Juvenon sells acetyl carnitine plus lipoic acid supplements degenerative diseases. The optimum in- lipid found only in mitochondria). Oxi- and does clinical trials on them. B.N.A.’s founder’s stock was put in a nonprofit foundation at the founding in 1999. He take of each micronutrient necessary to dative damage to DNA, RNA, proteins, is director of Juvenon’s Scientific Advisory Board, but he has maximize a healthy lifespan remains to and lipids in mitochondrial membranes no stock in the company and does not receive any remu- be determined and could even be higher contributes to this decay (9, 13–16) and neration from them. than the current RDA, particularly for leads to functional decline of mitochon- *E-mail: [email protected]. some populations (7, 10). For example, dria, cells, tissues, and eventually organs © 2006 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0608757103 PNAS ͉ November 21, 2006 ͉ vol. 103 ͉ no. 47 ͉ 17589–17594 Downloaded by guest on October 2, 2021 reduced in the mitochondria to a potent resistance to oxidants compared with a and diabetes (48) in humans and colon antioxidant. LA is also an effective in- standard or magnesium-supplemented cancer in mice (57). Selenium deficiency ducer of Ϸ200 phase 2 antioxidant and diet (32). This evidence suggests that in mice induces genes linked to DNA thiol-protective enzymes, including those supplementation programs should be damage and oxidative stress (58), and it required for glutathione synthesis (17– considered, because there is little risk of has been suggested that selenium pro- 19). ALC and LA when added as a sup- magnesium toxicity (5). A standard mul- tects against cancer (59, 60). Potassium plement can act, in some cases synergis- tivitamin–mineral (MVM) supplement in table salt in elderly men was associ- tically, to restore much of the lost does not contain sufficient magnesium ated with a 40% decrease in cardiovas- mitochondrial function in old rats (13– (or calcium) because it would make the cular disease compared with normal 16), which appears to rejuvenate the supplement too bulky. table salt in a randomized controlled mitochondria and improve cognition and trial (RCT) (61). Omega-3 fatty acid other functions (9, 13–16). Vitamin D Deficiency. The dark skin of deficiency is associated with melanoma One possible mechanism of mitochon- people indigenous to southern India, and other cancers (62) as well as cogni- drial decay is that, with age, increased Africa, and other tropical regions pro- tive dysfunction (63). The effect of B oxidative damage to mitochondrial pro- tects against excessive UV light expo- vitamin deficiency on mitochondria was teins causes structural deformation of key sure from the sun. On the other hand, reviewed recently (64). Vitamin B12 de- enzymes that lowers their affinity for the dark skin interferes with the formation ficiency is common in the population enzyme substrate (16). Feeding old rats of vitamin D in the skin, which requires (4); it is associated with cognitive dys- the substrate ALC with LA for a few UV light. Thus, dark-skinned people in function (65) and multiple sclerosis (66) weeks decreases oxidative damage, allow- northern latitudes are often vitamin D- and induces chromosome breaks (11). ing the synthesis of new carnitine acyl deficient. For example, African Ameri- The cognitive dysfunction associated transferase with normal binding affinity cans as a group are particularly deficient with B12 deficiency improved with sup- (Km). This partially restores mitochondrial in vitamin D (33, 34). In The Nether- plementation within the first year of on- function; decreases oxidants, neuronal lands there is a very high level of vita- set (67). Folate deficiency also causes RNA oxidation, and mutagenic aldehydes; min D deficiency during pregnancy in chromosome breaks (11, 56, 68) and is and increases rat ambulatory activity and dark-skinned women (35, 36). Inade- associated with several human cancers cognition (13–16). ALC and LA are not quacy is prevalent in Caucasians as well (69, 70). Marginal thiamine deficiency in thought of as micronutrients, because they (37). Vitamin D deficiency has been es- rats induces the formation of colonic can be synthesized in the body, but they timated to account for 29% of cancer aberrant crypt foci, a preneoplastic le- are illustrative of many normal metabo- mortality in males (38) and has been sion in a model for detecting colon car- lites that may be beneficial in the elderly. strongly associated with colon, breast, cinogens (64). Thiamine deficiency is The association of several micronu- pancreatic, and prostate cancer (38–44). also associated with brain dysfunction
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