Full-Body Peril. aurie s seizures, which caused her arm to
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1 38 THE MANY MANIFESTATIONS OF TUBEROUS SCLEROSIS COMPLEX: Tubers in the brain that cause autism and epilepsy // Holes that pock the lungs // Tumors that disrupt kidney function // The understanding of which could unlock treatments for other, more common afflictions. Full-Body Peril by anita slomski // illustrations by daniel chang aurie s seizures, which caused her arm to L jerk and mouth to go crooked, started when she was one. Neurologists couldn t identify a cause, nor did they understand why, three years later, she had learned only 12 words. Finally, at age seven, Laurie was diagnosed with tuberous sclerosis complex, a rare genetic disease now believed to afflict one in every 6,000 people. By then, Laurie had a large blisterlike bubble on her nose, as well as a red butterfly pattern on her face. When she was 28, tumors on her kidneys started to bleed. The pain was excruciating, and eventually surgeons had to remove all of one kidney and part of the other. Then, in her mid-thirties, she developed a lung disease, also an outgrowth of TSC, that could ultimately collapse her lungs and kill her. Like half of all people with TSC, Laurie has cognitive limitations. She has trouble reading and understanding what people say to her, and it s not easy for her to make decisions about what to wear or which groceries to buy. Other TSC sufferers are in much worse shape. Almost all suffer from intractable epilepsy, and many are profoundly retarded or autistic. Yet there are also those who have scant symptoms, usually skin rashes or bumps, and who may not even know they have the disorder. For one sufferer, a physician, the first sign of trouble came when she developed asthmalike shortness of breath at age 40. Only then did a CT scan reveal the abnormal cells invading her lungs. Yet as bizarre and obscure as TSC has been a typical rare disease, little known beyond its small circle of sufferers, family members and caregivers it has recently emerged as something else entirely. The disease s hallmarks are noncancerous growths that appear in multiple organs and the tuber-shaped abnormalities masses of abnormal cells and disorganized tissue that develop in the brain. Eight years ago, when researchers stumbled onto how two proteins cause the uncontrolled cell growth of TSC s tumors and tubers, oncologists took notice. Cancer biologists are intrigued by why mutations in the TSC proteins produce tumors that are benign or actually regress, says neurologist Elizabeth A. Thiele, director of the Herscot Center for Tuberous Sclerosis Complex at Massachusetts General Hospital. What causes the cells to grow into a tumor and then sometimes go away? Other aspects of the odd disease also caught researchers attention. Nine out of 10 people with TSC have epileptic seizures, and answers about how defective genes create signaling abnormalities in brain cells might hint at what causes epilepsy in those who don t have TSC. And the disease also has a link to autism, one of medicine s most enduring mysteries. We don t know what causes autism in most kids, Thiele says. But if your kid has TSC and is autistic, you know that the disease is responsible. So we think we can extend what we learn about TSC to other kids with autism. Research has been helped by a ready-made treatment, an immunosuppressant already approved for people who have kidney transplants that also acts on the cellular pathway that includes TSC proteins. We were immediately able to move from understanding the root cause of TSC to clinical trials for treating it, says Cheryl L. Walker, professor of carcinogenesis protomag.com // winter 11
2 39 winter 11 // protomag.com
3 40 at the University of Texas MD Anderson Cancer Center. Though not a cure, the drug rapamycin seems to shrink the benign tumors of TSC, and cancer researchers wonder whether it might do the same for malignancies, perhaps combined with drugs that actually kill the proliferating cells instead of making them dormant. The same treatment might also prevent seizures in the general population, particularly after brain injury, rather than just suppressing them, as antiepileptic drugs do. While TSC itself still baffles clinicians more than a third of people with the disease are misdiagnosed, sometimes for decades it has become what Thiele, at least, describes as an intriguing disease. tubers themselves that generate seizures. But it s more likely that the abnormal tissue of the tuber somehow irritates or disrupts the normal-seeming brain tissue around them, says pediatric neurologist Michael Wong, director of Washington University s Tuberous Sclerosis Clinic in St. Louis. Neurons within or surrounding the tubers generate abnormal electrical activity that builds up and results in seizures. Epilepsy in people with TSC is often more severe than other forms, and two-thirds of TSC sufferers experience seizures that respond poorly to medication. Babies with TSC are at particular risk of developing a catastrophic type of epilepsy called infantile spasms, which may result in profound intellectual disability in two-thirds of those who have it. About half of those with TSC have some sort of intellectual or cognitive impairment, ranging from mild learning disabilities to severe autism or retardation. Though the number of tubers in the brain partly predicts the severity or type of intellectual or cognitive problem, location may also matter. Psychiatrist Patrick Bolton has found that The distinctive tuber-shaped growths that appear throughout the cerebral cortex (the brain s outer layer) in people with TSC were first described by the French physician Désiré-Magloire Bourne ville in And when sliced open, TSC tubers indeed resemble the firm, white flesh of a potato. They re made up of abnormally shaped and dysfunctional brain cells that form during fetal development, and nearly everyone who has TSC has brain tubers. Some people may have just one or two, while others have so many they cover large areas of the brain. Yet while these tubers may calcify and become hard, they do not proliferate and grow, and they re found only in the brain. Some of the far-flung maladies of TSC are directly related to these brain masses. In the case of epilepsy, for example, it may be the protomag.com // winter 11
4 tubers in parts of the brain such as the temporal lobe regions appear to increase the likelihood of developing autism. The temporal lobes contain neuronal networks that specialize in processing information about faces, facial expression and the direction of someone s gaze, which give clues about the social world, says Bolton, professor of child and adolescent psychiatry at King s College London. Tubers causing abnormal electrical discharges in this area may prevent the brain from learning how to process such information, leading to autism spectrum disorder, which may affect as many as one in two children with TSC. Understanding how that happens is helping researchers grasp how autism may develop in children who don t have TSC. Since the discovery of dysfunctional biochemical pathways in TSC, we ve begun to find problems with other genes in those pathways that may also lead to autism, Bolton says. Though the effects of TSC tubers may explain the disease s most common manifestations, abnormal cell masses develop outside the brain, causing a laundry list of symptoms. Unlike TSC tubers in the brain, these noncancerous tumors show up elsewhere, can appear after birth and may continue to grow throughout a person s life. Kidney tumors called angiomyolipomas, or AMLs, are particularly common, and while they aren t normally a problem, some may hemorrhage or grow very large. (One of Thiele s patients, in her forties, has an AML 20 centimeters square that has obscured her kidneys and swollen her abdomen to make her seem hugely pregnant.) The blood vessels feeding AMLs may become leaky and malformed, inviting aneurysms that can rupture, causing intense pain and potentially fatal bleeding. Surgeons can t remove an AML without the significant risk of destroying kidney function, but they can do a procedure called embolization that cuts off the blood supply to the main vessel feeding the tumor, causing it to wither. Even then, however, an AML may start to grow again, and some people have too many AMLs to count. In another quirk of TSC, the same abnormal smooth muscle cells that cause AMLs may appear in the lung, resulting in a potentially fatal disease called lymphangioleiomyomatosis (LAM), which causes holes to develop in the lungs. LAM almost always All of the complex s ailments, from epilepsy and autism to kidney and lung problems, seem to stem from mutations in two genes, TSC1 and TSC2. strikes women during childbearing years, and if it progresses rapidly, a lung transplant may be the only way to save a patient. Typically, cells from benign growths don t spread to other organs that s a hallmark of cancer. And while these cells do metastasize, it s not as simple as kidney cells spreading to the lung, because a third of women with LAM don t have kidney tumors, says oncologist Elizabeth Henske, a professor at Harvard Medical School and director of the Center for LAM Research and Clinical Care at Brigham and Women s Hospital in Boston. It may instead be that the cells spread to both the kidney and the lung from some mysterious site we don t know of yet. But whatever their path, the fact that LAM cells may also appear in a lung transplanted to replace the failing, LAMinfected organ suggests the cells are indeed metastasizing, says Henske, whose research has found that genetic mutations in AML and LAM cells are identical. And, in another link to cancer, both kinds of TSC cells produce many of the same proteins that melanoma cells do. Unlike cancer, however, LAM can suddenly stop progressing, especially after menopause. (Estrogen appears to help these cells migrate.) All of these ailments, from epilepsy and autism to kidney and lung problems, seem to stem from mutations in two genes, TSC1 and TSC2, that scientists discovered during the 1990s. But it wasn t until years later that researchers unraveled the process through which tuberin and hamartin the proteins synthesized by TSC1 and TSC2, respectively cause the runaway cell growth that gives rise to TSC tubers and tumors. When they work properly, tuberin and hamartin team up to provide an essential cell function. A cell makes decisions winter 11 // protomag.com
5 42 turn on another protein, Rheb, which activates still another, mtor. This final, pivotal protein then signals the cell to take up more nutrients, produce more proteins, and grow and divide. When either TSC1 or TSC2 is defective, it interferes with the braking mechanism and keeps mtor switched on all the time, letting cells divide uncontrollably and leading to the development of TSC s tubers and tumors. The mtor pathway exists in every cell of the body and serves as a master switch to regulate normal cell growth, development and survival. In the brain, for example, mtor controls the synthesis of proteins needed to form synapses and strengthen synaptic connections, important in learning and memory. Problems with the pathway also seem to be involved in diabetes, cardiovascular disease, Alzheimer s disease, cancer and obesity. through signaling pathways, a logical network of proteins that bind to other proteins to send the cell instructions to grow, divide or die, says Lewis C. Cantley, professor of systems biology at Beth Israel Deaconess Medical Center in Boston. The job of tuberin and hamartin is to act as a brake when a cell is in trouble if, for example, it s running out of nutrients or oxygen. The TSC proteins suspend the growth of the cell, which would die if it kept trying to grow, Cantley says. It s an ancient mechanism even yeasts have it and it allows the cell to do everything it can to repair itself. In 2002, Cantley was trying to learn how another protein, Akt which operates in the same cellular pathway as tuberin and hamartin and has been linked to several human cancers transforms a cell to make it cancerous. When a cell wants to divide and grow, growth factors that bind to the cell s outer surface activate Akt, which then passes a signal to tuberin and hamartin to suspend their braking function. With those proteins turned off, the growth signal from Akt proceeds along the pathway to But the discovery of mtor s role in TSC wasn t the protein s first appearance in medical research. Years earlier, researchers had found that it plays a critical role in modulating the function of the immune system, particularly in lymphocytes, a type of white blood cell that attacks viruses, bacteria and other foreign bodies. Lymphocyte function needs to be suppressed in people who ve had kidney transplants, to prevent lymphocytes from attacking and rejecting the new organs, and it turned out that a drug, rapamycin, developed for immunosuppression, worked by inhibiting mtor. (The drug came first, and the protein is actually named for it mtor is an acronym for mammalian target of rapamycin.) Because rapamycin can head off the unrestrained cell growth caused by problems with TSC proteins, researchers immediately saw it as a potential therapy, and several clinical trials quickly got under way. The first, begun in 2002 at Cincinnati Children s Hospital, examined rapamycin s effect on AMLs and LAM in the kidneys and lungs of 25 TSC patients. The results, published in 2008, showed that kidney tumors shrank significantly during the year of therapy, though most returned to their original size when patients stopped taking the drug. For the 11 trial participants who had LAM, rapamycin improved their lung function, an effect that persisted for some even after the trial ended. Subsequent trials have gauged the impact of rapamycin as a treatment for epilepsy and other neurological manifestations of TSC. Several researchers have shown in animal trials that the drug may be able to prevent epilepsy. When infant mice engineered to have brain disorders resembling TSC are given rapamycin, they usually do not develop seizures, according protomag.com // winter 11
6 Once we figure out what drugs to use in TSC to make those cells die, rather than just stop growing, we should be able to extrapolate that regimen to cancer. to research by Washington University s Wong and others. The abnormal cell changes in the brains of the mice are also prevented, says Wong, who has also used rapamycin to stop seizures in mice with brain injuries unrelated to TSC. The cellular changes from brain trauma abnormally activate the mtor pathway and can lead to seizures, he adds, noting that blocking those changes might also head off seizures caused by stroke. One recent breakthrough, however, may reverse these neurological effects by shrinking the tubers in the brain that cause them. The drug Afinitor (everolimus), which works similarly to rapamycin, gained FDA approval for treating tubers after a study showed that 75% of patients experienced tuber reduction by 30% or more while taking the drug. Many researchers now think the most effective treatment for TSC will be to give rapamycin to stop the hypergrowth of cells and to combine it with another drug that will selectively kill abnormal cells. We d like to be able to give a short-term, combination therapy to kill the cells, and then use it again periodically if regrowth occurs, Henske says. Once we figure out what drugs to use in TSC to make those cells die, rather than just stop growing, we should be able to extrapolate that regimen to cancer. I really believe we ll make progress against cancer by successfully treating TSC. Other research is focused on finding potential drug targets related to mtor that may be more specific to TSC and that could result in therapies without the side effects of an immunosuppressive drug, which can leave patients prone to infections. Geneticist and oncologist David Kwiatkowski at Brigham and Women s Hospital, who found the TSC1 gene, has had some tentative success with metformin, a common and safe diabetes drug that appears to interrupt the mtor pathway by activating a kinase an enzyme that chemically modifies other proteins called AMPK. An enzyme called COX-2 also appears to be activated in LAM and AML tissue, so we are trying out inhibitors of COX-2, which are also welltolerated drugs, Kwiatkowski says. And to kill the abnormal cells created by TSC, Kwiatkowski is experimenting with a drug that prevents the breakdown of protein in a cell. Cells lacking normal TSC1 and TSC2 genes make too much protein, which creates a stress response in the cell, Kwiatkowski explains. By inhibiting the cells ability to break down the protein, the stress is made worse and could cause the cells to die. All this progress after decades during which no therapy seemed possible has energized the scientists who have toiled to understand this rare disease. We know TSC tumors take years or decades to develop and they are quite predictable, Kwiatkowski says. With a drug like metformin that a patient can take for the rest of her life with very few side effects, we would have a very effective treatment if started early enough. Even if therapy reduces the rate of growth of the tumors by only 20% per year, she may never develop AML or LAM, and that would be a terrific outcome. Dossier 1. The Tuberous Sclerosis Complex, by Peter B. Crino et al., The New England Journal of Medicine, Sept. 28, This review article details the wide array of clinical features of TSC, along with the hypothesis that TSC takes on the metastatic characteristics of cancer as benign cells with mutations in their TSC genes migrate from the kidneys to the lungs. 2. Mammalian Target of Rapamycin (mtor) Inhibition as a Potential Antiepileptogenic Therapy: From Tuberous Sclerosis to Common Acquired Epilepsies, by Michael Wong, Epilepsia, January TSC research has opened a window into potential therapies for cancer and epilepsy, and this author makes the case that the cellular pathway disrupted in TSC may also contribute to nongenetic forms of epilepsy holding promise that inhibiting the pathway may offer a way to prevent seizures. 3. Living With TSC (www2.massgeneral.org/livingwithtsc/). This comprehensive and interactive Website by Massachusetts General Hospital includes interviews with TSC scientists on the latest research and current treatment and diagnosis options, along with the voices and stories of families coping with TSC. 43 winter 11 // protomag.com
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