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Published On May 3, 2012

BASIC RESEARCH

A Matter of Taste

Science is unraveling the biological factors that determine food preferences. Next: making people like what's good for them.

HOW PEOPLE PERCEIVE AND RESPOND TO THE TASTE OF FOOD is largely a matter of evolution. We’re born loving sugar because it signals the presence of carbohydrates that fuel the body. We want salt because it maintains our cells’ electrolyte balance. Savory alerts us to amino acids, the building blocks of proteins. Bitter warns against ingesting toxic, noxious chemicals in plants, and sour saves us from spoiled, fermented food. Yet not all tasters get the same message. John Hayes drinks unsweetened black coffee but shuns grapefruit. His wife loves grapefruit but abhors black coffee. Their daughter likes both and sometimes prefers grapefruit to cheesecake.

Hayes is director of the Sensory Evaluation Center at Pennsylvania State University, and based on his research, he thinks he can relate those varying preferences to underlying biological differences in how tongues detect bitter compounds. Such innate variations, mostly determined by a person’s genetics, affect how responsive taste buds are to particular food molecules, as well as how many taste buds there are, and so how strong a signal they send to the brain. Varying perceptions of the five basic tastes—bitter, sweet, salty, sour and savory (or umami, a Japanese word for “delicious”)—affect food likes and dislikes, which influence our food choices.

Inborn attractions and aversions served humans well when the most important thing was getting enough food and not being poisoned by it. Yet our needs have evolved, and it would be ideal now if taste encouraged healthy food choices—rather than pushing people away from broccoli, for instance, which some find repulsively bitter, or drawing us to fattening sweets and carbohydrates. Indeed, bitter compounds also contain beneficial vitamins, antioxidants and flavonoids.

Scientists have only recently begun to understand how the tongue, much less the brain, responds to taste and how genetic variations affect its response. Now, as they trace connections among taste, flavor and food choices, they’re finding that people’s innate predispositions don’t always predict which foods they will actually like or dislike, and that environmental factors, including a mother’s choices passed along in amniotic fluid, also play a role. As researchers parse the interplay of all of these factors and their impact on health, some are looking ahead to a time when it may be possible to entice people toward foods they are hardwired to avoid and away from others they enjoy to an unhealthy extreme.

A LARGE PART OF THE GUSTATORY SYSTEM, WHICH GOVERNS what and how we taste, is visible on any human tongue. There are small, mushroom-shaped structures called papillae that contain globular clusters of taste buds. Each taste bud in turn has 50 to 150 taste cells, each of which is studded with proteins known as chemoreceptors that detect only one of the five tastes. Chemoreceptors bind to a specific type of food chemical, variously known as a tastant, taste stimulus or ligand. For example, natural sucrose and similarly shaped molecules in artificial sweeteners are tastants that connect to sweet receptors, and when they make their wonted links, they trigger a reaction that sends a signal of sweetness to the brain. That message travels along a cranial nerve from the tongue to the medulla, in the brain stem, which connects to other brain regions involved in appetite, emotion and cognition.

Scientists knew much less about the physiology of taste 80 years ago, when DuPont chemist Arthur L. Fox made an accidental discovery. Fox was transferring a newly synthesized compound, phenylthiocarbamide, or PTC, to a container, and some of the powder wafted into the air. A colleague tasted something horribly bitter, but Fox detected nothing. Curious, he gave samples to other people, most of whom also thought it ghastly. But about a quarter of them, like Fox, found it tasteless. Fox and geneticist A.F. Blakeslee then took PTC to a scientific meeting and observed a 2.3-to-1 ratio of tasters to nontasters—close enough to the 3-to-1 inheritance pattern of dominant to recessive characteristics, as with Gregor Mendel’s peas, to indicate that nontasting was a recessive trait.

Yet why would humans have evolved in such a way that most were repelled by a nonnatural substance? The answer, which didn’t emerge until the 1950s, was that disliking PTC—and a related synthetic chemical, PROP—was a kind of accident. The innate aversion of those who could taste those compounds was to bitter chemicals, called glucosinolates, in cruciferous vegetables such as kale and brussels sprouts (PTC happens to mimic natural glucosinolates). One glucosinolate, goitrogen, is toxic to the thyroid in large quantities, so it made sense, in evolutionary terms, for people to have a sensitivity to it. However, in smaller amounts, other glucosinolates may help ward off cancer.

By the 1960s, a few scientists had confirmed what the earlier research seemed to predict—that whether someone could taste PTC/PROP predicted how many foods they disliked. But that observation was largely ignored until the 1990s, when Linda Bartoshuk, then at Yale University and now at the University of Florida, discovered additional layers of complexity.

Bartoshuk found that some people qualified not only as tasters but as “supertasters,” at the opposite end of the spectrum from nontasters. Rather than determining whether people could detect low concentrations of PROP—the acid test dividing tasters from nontasters—Bartoshuk looked at how intensely people perceived higher concentrations. Using sound and light as a frame of reference, she discovered a wide range of intensities. “Most of us live in a world of pastel tastes, but about 25% of us have neon tastes,” she says. To those supertasters, bitter is more bitter, salt is saltier and sugar is sweeter—and food likes and dislikes tend to be more extreme.

BARTOSHUK'S WORK LED OTHERS TO EXPLORE HOW GENES INFLUENCE TASTE. In subsequent studies, scientists found that each type of tastant—bitter, sweet, salty, sour or umami—triggered a different kind of chemoreceptor, and the observation of differences in how tastes are perceived suggested that those receptors might vary from person to person, because of variations in the genes controlling the receptors.

In the late 1990s, researchers began to identify those receptor genes, first in mice and then in humans. They knew that different strains of mice had distinct preferences for sweet and bitter, judged by how voraciously they would lap up sugar water of a particular concentration and whether they would shun water laced with bitter compounds. By then, human and mouse genome sequencing projects were well under way, and in 2000, Charles Zuker, a neuroscientist at Columbia University, working with National Institutes of Health scientists, identified a family of bitter receptors and showed that the mouse genes for those receptors came in taster and nontaster variants that resulted in different sensitivities to bitter chemicals.

Bitter receptors (and also those for sweet and umami) belong to a class called G protein–coupled receptors (GPCRs), with seven loops that span cell membranes, and have an extracellular extension like a Venus flytrap. This flytrap can bind to a chemical of a particular shape floating by on the tongue in lock-and-key fashion. When a bitter compound fits the lock, that connection causes the taste cell to send a signal to the brain.

In the early 2000s, researchers used the results of the recently sequenced human genome to identify the human bitter taste gene TAS2R38, which governs the PROP/glucosinolate receptor. Subsequent studies showed that minute inherited differences in the gene change the shape of the receptor’s binding pocket—the lock in the lock-and-key connection in the flytrap. About one in four people (supertasters) receives two genes (one from each parent) that produce a receptor that binds strongly to PROP; another 25% (nontasters) receive genes that yield a receptor that binds weakly, if at all; the rest (mid-tasters) receive one of each.

Several labs have now shown that these small genetic modifications change the response to taste compounds, and scientists have engineered mice to tweak their sweet and bitter genes and alter their food preferences. “Taste is greatly affected by the activity of our receptors,” says Zuker. “And because receptors vary from person to person, so does the way we experience taste.” That means that people live in separate taste universes, and each person’s individual constellation can have much to say about overall health.

Yet these genetic differences alone don’t explain the wide variation in bitter perception, which may range from absolute distaste to active appreciation. “We can’t separate high tasters from mid-tasters with a genetic test,” says Hayes. And only certain bitter keys—PROP and the glucosinolates from kale and related vegetables—fit the binding lock of the protein produced by the TAS2R38 gene. It turns out humans have, in addition to PROP, some two dozen other bitter receptors. At least some of the genes for those receptors also have multiple versions, further explaining the wide variations in how people perceive different flavors.

Some of the most telling information about how a grab bag of genetic differences relates to taste comes from a study published in the March 2011 issue of Chemical Senses. Hayes, Bartoshuk and their colleagues examined DNA collected from participants and analyzed the genes associated with several bitter receptors to create a genetic profile of each participant. Then the researchers asked the participants to taste samples of three bitter drinks—unsweetened grapefruit juice, instant espresso and blended Scotch whisky—and rate the intensity of each sample. Some participants rated coffee as tasting twice as bitter as others found it, but not all of those same participants found grapefruit or Scotch to be exceptionally bitter. These broad variations arose because there are so many genes for bitter receptors, making it possible for each person to inherit an idiosyncratic combination. Hayes and his team found that an unknown bitter compound in grapefruit juice, possibly naringin, triggers the bitter receptor TAS2R19. Alcohol triggers both TAS2R16 and TAS2R38, and coffee may activate TAS2R3, TAS2R4 or TAS2R5.

THIS LATEST RESEARCH IS HELPING TO EXPLAIN HOW PARTICULAR GENES appear to relate to specific tastes, and the combination of gene variants that someone inherits seems likely to influence which foods that person will crave or avoid. But another factor, visible on the tongue, also affects the relative intensity of how tastes are experienced. When Bartoshuk discovered supertasters, she noticed that they had more papillae than non- and normal tasters. Having extra papillae also affects the perception of a food’s flavor—a quality that takes into account the pain of hot chili, the cool of mint, the texture of whole grains and the “mouth feel” of fat. And it turns out that papillae contain nerve fibers with receptors for touch—and those who have larger numbers of papillae, with additional nerve receptors, tend to experience foods more intensely.

That’s another reason, Bartoshuk says, that supertasters are likely to find bitter vegetables, sweet desserts and fatty, creamy foods unpleasantly vivid. They tend to gravitate toward mild food, eating fewer ribs, fries and desserts, but also less broccoli. That diet could give supertasters lower risks for obesity, diabetes and cardiovascular disease but might leave them lacking the protection against cancer that some vegetables may provide.

While it’s easy enough to test these hypotheses in genetically altered mice, it’s been difficult to establish definitive connections between high- and low-tasting receptors and human behavioral choices. The evidence that such links exist is strongest between bitter and vegetables, largely thanks to work by Valerie Duffy, a registered dietitian at the University of Connecticut. In a November 2010 study, Duffy, Bartoshuk and Hayes directly linked differences in vegetable intake to the TAS2R38 gene. Adults with one or two copies of the taster gene—a group that, in previous research, experienced more bitterness in vegetables in taste tests—reported eating about 25% less vegetables than those with two copies of the nontaster gene.

Research on other types of food has found smaller effects, and none proves that taste genes determine food choices. Among the disparate findings are that adult supertasters like sweet foods somewhat less than others do, but supertaster children like them more. Among college males, supertasters are thinner. Supertasters have better lipid profiles, suggesting lower cardiovascular risk. Older male supertasters who report consuming fewer vegetables have more colon polyps (a risk factor for colon cancer).

GENES AND THE RECEPTORS THEY CONTROL ARE ONLY PART OF THE EQUATION because they interact with environmental, behavioral and cultural influences. For example, illness and smoking can dull taste receptors, Grandma’s home cooking can make you love brussels sprouts, and fast foods can get you so accustomed to a lot of salt that regular food tastes bland. So food preferences are not predetermined, and in fact they’re quite malleable. Both early and late in life, there are windows of opportunity to modulate proclivities to avoid or embrace particular foods, says Gary Beauchamp, a taste researcher at the Monell Chemical Senses Center in Philadelphia.

“There’s a huge amount of data from animal studies showing a transfer of flavor via amniotic fluid from the mother to the fetus, and in rats, pigs and mice, babies will more readily eat foods their mothers ate,” Beauchamp observes. “We have found that human babies have similar tendencies.” The same is true of the foods a nursing mother eats, because flavor compounds dissolve in breast milk. “The foods a woman eats during pregnancy and nursing can have long-term implications for children’s preferences later in life,” he says.

Adults can also modify their preferences for salts, as Beauchamp demonstrated during the 1990s. Over a period of six to eight weeks, he gradually reduced the level of sodium in soup given to a panel of human subjects. In time, the salt concentration the testers had thought was ideal came to be perceived as too salty. “In theory we could use that approach to shift the whole population down to levels closer to that recommended by U.S. dietary guidelines,” he says.

Relearned perceptions of other tastes might one day help people overcome genetic proclivities—or drugs or food additives could be developed that make healthy but unpopular food choices more palatable. The goal, says Columbia University’s Zuker, is “to help people enjoy the things that make our sensory experiences rich in a healthy, productive way. If we could modulate the activity of taste receptors, we could perhaps help with serious problems in our dietary world.”

 

DOSSIER

1. “Common Sense About Taste: From Mammals to Insects,” by David A. Yarmolinsky, Charles S. Zuker and Nicholas J. P. Ryba, Cell, Oct. 16, 2009.The authors take us on a tour of the tongue and through a series of animal experiments to demonstrate the “logic” of how tastes are coded and transmitted to the brain.

2. “Nutritional Implications of Genetic Taste Variation: The Role of PROP Sensitivity and Other Taste Phenotypes,” by Beverly J. Tepper,Annual Review of Nutrition Volume 28, 2008. This review provides a historical overview of the discovery of genetic variations in bitter taste perception and evaluates the conflicting evidence for a relationship of genetic variations in taste receptors to food choice, diet and health.

3. “Molecular Mechanism of the Sweet Taste Enhancers,” by Feng Zhang et al., Proceedings of the National Academy of Sciences, March 9, 2010.This study of a sweet enhancer demonstrates how researchers can use molecular biology and drug development to produce new compounds that can reduce the amount of sugar added to food and block the bitter taste of medicines, artificial sweeteners and vegetables.

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